Running-related hamstring injuries: a neuromuscular approach

Running-related hamstring injuries: a neuromuscular approach Gisela Sole1, Stephan Milosavljevic1, S. John Sullivan1 and Helen Nicholson2 1

Centre for Physiotherapy Research, School of Physiotherapy, University of Otago, Dunedin, New Zealand 2 Department of Anatomy and Structural Biology, University of Otago, Dunedin, New Zealand Hamstring injuries are common in running and sprinting sports and have a high recurrence rate. Prevention and management of these injuries has focused on traditional outcomes of strength, flexibility and endurance. The aim of this review is to explore the stabilising function of the hamstring muscle group, described as increasing the stiffness of the sacro-iliac and the knee joints during weight acceptance of stance. Loss of stability of segments proximal or distal to the hamstring muscles may lead to altered muscle recruitment, potentially increasing the loading of this muscle group and, thereby, posing an increased injury risk. Intrinsic risk factors to be considered are previous knee, groin or lumbopelvic injuries; extrinsic factors include footwear and training surfaces. The effect of physiotherapy interventions on the stabilising function of the hamstrings needs to be investigated. Such research will contribute to a clearer understanding of the reasons for the high injury recurrence rate of this muscle group. Keywords: function, hamstring muscles, injury, motor control

Introduction Non-contact hamstring muscle strains have received much attention in a range of publications during the past 20 years. Measures to indicate injury risk levels and outcomes following these injuries have focused mainly on muscle strength, flexibility and endurance.1 However, these have not clearly distinguished subjects with hamstring injuries from control subjects.2,3 While some programmes based on strength and flexibility have been shown to reduce the seasonal incidence of hamstring injuries,4–6 the injury remains a common occurrence, with reported incidences varying between 20 and 35% of all injuries incurred during one season of various sports codes.7,8 These include soccer,9 rugby and Australian Rules football,10 cricket11 and track and field.12 A more recent approach to management of hamstring injuries has highlighted the putative role of trunk stability in potentially reducing recurrence of this injury.13 Although measures of trunk stabilisation or neuromuscular control were not assessed, the authors concluded that enhanced neuromuscular

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control of the lumbar spine and pelvis may reduce the incidence of recurrence.13 However, the mechanism whereby this would occur was not established. In another study, decreased movement discrimination during open kinetic chain movements has been shown to increase the risk of incurring a hamstring injury.14 Thus, it appears that factors other than hamstring muscle strength, flexibility and endurance need to be considered as contributors to first-time and recurrent injuries of these muscles. Consistent findings from prospective and retrospective surveys indicate that a previous history of injury of the hamstring muscle group increases risk for further injury.7,15–19 Other injuries, such as knee injury, osteitis pubis16 and calf muscle injury20 also place the player at risk of a hamstring injury. Although anecdotal evidence has suggested that either lumbar spine pathology21–23 or sacro-iliac dysfunction24 can predispose people to hamstring injuries, this has not been confirmed in a prospective study.16 Observations may be confounded by the fact that low back pain is also common in various

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sporting codes.25 Therefore the mechanism that putatively links injuries to other joints or segments to an increased risk of a hamstring injury is not clear. Aspects of altered muscle recruitment have been considered in conjunction with pain or injuries of regions or structures linked to the hamstring muscles, such as the low back,26 groin,27 pelvis28 and the knee joint.29,30 Such research and anecdotal evidence suggests an alteration in recruitment of the hamstring muscle group in the presence of loss of stability elsewhere in the kinetic chain. Loss of stability could be due to other injuries (intrinsic factors), as well as extrinsic factors, such as ground surface or footwear. To understand how a neuromuscular approach is important in the reasoning and management of hamstring injuries, the function of this muscle group needs to be explored. The aims of this article are thus to review the present research on the function of the hamstring muscles and to determine the effect of related segment injury on this function. Such insight will be used to propose additional strategies that need to be considered in future research and in management of hamstring injuries.

Function of the hamstring muscle group The literature most commonly describes the function of the hamstring muscles as having a tonic role contributing towards torque production of hip extension and knee flexion during gait and running.31 The role of the eccentric contraction during the terminal swing phase of walking and running has been highlighted as decelerating the tibia before heelstrike.32,33 A phasic (postural) role for the hamstrings has been described as stabilising the pelvis during standing and the stance phase of gait in conjunction with gluteal and abdominal muscles.34 The stabilising function of the hamstring muscles group has been considered relative to joints related directly or indirectly to its insertion and origin, namely the sacro-iliac joint (SIJ) and the knee joint. Although it may also have a stabilising role towards the hip joint, this has not been investigated. The hamstring muscle group has been described as a dynamic stabiliser of the knee joint, particularly with reference to preventing anterior shear of the tibia during loading, and supporting the role of the anterior cruciate ligament.35 The underlying premise is that a proprioceptive mechanism exists between the anterior cruciate ligament and the thigh musculature which regulates hamstring activity during knee extension movements.36

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It has been proposed that the erector spinae muscles, the deep lamina of the thoracodorsal fascia, the sacrotuberous ligament and the biceps femoris muscle are part of a deep longitudinal system that improve functional stability of the SIJ.37 This hypothesis was initially based on findings of a cadaveric study demonstrating that tension in the biceps femoris increased tension within the sacrotuberous ligament. This increased tension is theoretically considered to increase stiffness of the SIJ.38 A more recent in vivo study with six healthy female subjects showed that voluntary sub-maximal contraction of the gluteus maximus, erector spinae and hamstring muscles respectively, increased SIJ stiffness, as inferred by colour Doppler imaging with induced oscillation of the ilium relative to the sacrum.39 This increased SIJ stiffness with hamstring contractions may be directly due to mechanical effects via the anatomical attachment of a portion of the long head of biceps femoris on the sacrotuberous ligament, and their common attachment on the ischial tuberosity. Contraction of the hamstring muscles can therefore have an effect on SIJ stiffness, potentially contributing towards dynamic stabilisation of the SIJ during functional movements and gait.40 The function of the hamstring muscles can also be considered as contributing towards maintenance of equilibrium and stability of the whole body. Electromyographic (EMG) activity of the hamstring muscles increases when leaning forwards from the ankle.41 During large asymmetric arm movements, the hamstring muscles are activated before the onset of the arm acceleration and deltoid EMG activity; similarly, during trunk rotation, the hamstring muscles of one leg contract together with the contralateral quadriceps muscles to stabilise the hips.42 Based on these findings, activation of the hamstrings appears to contribute towards maintenance of whole body stability as part of anticipatory postural adjustments when the centre of mass is challenged during dynamic kinematic activity. The main function of the hamstring muscle group during the final swing phase of gait has been described as eccentrically decelerating the lower leg.32,33 Further muscle functions during this phase also need to be considered. Muscle contraction during the final swing phase of gait serves to prepare for impact absorption, stiffen joints and decrease joint loading.43 Thus, the hamstring muscle contraction during the final swing phase of gait also functions to prepare and stabilise the extremity for

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weight bearing using feed forward control mechanisms. Besides contributing towards hip extensor and knee flexor moments, the function of the hamstring muscles can also be described as potentially contributing towards stability of the lumbo-pelvic segment, the knee joint, the lower kinetic chain and whole body stability. Its role in hip joint stability needs to be explored. How the stabilising function of the hamstring muscle changes following injury is currently unknown. However, findings of studies that have investigated recruitment of the hamstring muscles in subjects with disorders that increase the risk of hamstring injuries may contribute towards our understanding of the aetiology of these injuries.

Hamstring recruitment in subjects with related musculoskeletal disorders Surface EMG has been used in various studies to determine the activation patterns of gluteal and thigh muscles in subjects with low back or pelvic pain and knee disorders. In a group of subjects with low back pain (LBP) the onset of the gluteus maximus and biceps femoris during the swing phase while treadmill walking was earlier than that of a control group of subjects.44 Towards the end of the swing phase, the biceps femoris muscle exhibited increased activation in the group of subjects with LBP.44 In another EMG study, activation of trunk, pelvic and hamstring muscles of the supporting leg was monitored during contralateral hip flexion while standing in a group of male subjects with pelvic pain.28 On the symptomatic side, biceps femoris EMG activity occurred earlier than on the asymptomatic side when compared with control subjects.28 Thus, it appears that activity of the hamstring muscle group, specifically the biceps femoris, has an increased latency (earlier onset) and increased relative amplitude in some subjects with pelvic pain or LBP. Osteitis pubis, as confirmed by magnetic resonance imaging (MRI) of the pubic symphisis, has been associated with an increased risk of hamstring injury.16 In a study comparing muscle activation patterns in a group of subjects with groin pain with a group of asymptomatic controls, delayed EMG onset of transversus abdominus was found during a supine active straight leg raise task.27 This delay in onset of the deep abdominal muscle is similar to EMG patterns observed in subjects with pelvic28 or low back pain26 during weight-bearing tasks. More recently, it has been proposed that groin pain in athletes, which is a common symptom of osteitis

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pubis, may be associated with an underlying loss of stability of the pelvic rim.45 It is possible that the mechanism whereby osteitis pubis increases the risk of incurring a hamstring injury is due to loss of pelvic stability with associated increased hamstring recruitment. Further research studies are needed to substantiate or negate this hypothesis. Verrall et al. found that knee injuries increased the risk of incurring a hamstring injury in a cohort of footballers.16 Knee injuries were defined as anterior cruciate ligament reconstruction, previous lateral patellar dislocation or arthroscopic diagnosis of degeneration secondary to previous knee injury, such as posterior cruciate ligament deficiency.16 Deficits in neuromuscular control of thigh muscles have been associated with the aetiology of non-contact anterior cruciate ligament injuries.46 Increased hamstring activation and increased co-contraction with the quadriceps group have been observed in subjects with anterior cruciate ligament deficiencies during sub-maximal and maximal isometric knee extension,47 walking, running48–50 and lunging;51 and in subjects with increased knee laxity during static perturbations.52,53 Similarly, increased hamstring muscle recruitment (evident as earlier onsets or increased EMG amplitudes) has been observed in subjects with knee osteoarthritis during walking and stair climbing.54,55 Increased recruitment of the hamstring muscle group, either via the medial hamstrings or the biceps femoris, or both, therefore appears to be present in subjects with disorders challenging the stability of the lumbo-pelvic segment and of the knee joint. Thus, the mechanism whereby an injury within these segments increases the risk of a subsequent hamstring injury may be due to loss of stability. Based on the above studies, loss of stability in these areas may be associated with increased recruitment of this muscle group in the presence of these disorders. This increased recruitment, in turn, may be an underlying factor contributing towards the aetiology of hamstrings muscle injury. Extrinsic factors, specifically running surface and footwear, also have the potential to affect hamstring recruitment. Pinnington et al. showed that hamstring and vasti recruitment increased while running on soft, dry sand compared to a firm surface at the same speed.56 Furthermore, footwear has the potential to destabilise the lower leg57 and has been shown to affect hamstring recruitment during running.58 Specifically, it has recently been shown that an ‘anti-pronation orthotic’ increases the hamstring

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activity before heelstrike in some subjects.59 The authors of that study59 proposed that activity of some muscles can increase if an orthotic intervention does not support the ‘preferred movement path’. In an early study on the surface EMG of muscle groups during sprinting, Mann and Sprague60 suggested that athletes with previous hamstring injuries exhibited increased activity of this muscle during sprinting, as determined by higher hip extension and knee flexion moments. An unexplored possibility is that injuries of related body segments increases the risk of a hamstring strain by increased recruitment during functional activities. This increased recruitment could be a compensating mechanism for loss of stability at any location along the kinetic chain.

Loss of stability of the kinetic chain as underlying contributing factor towards hamstring injuries Functional stability integrates sensory, motor and central components and can be described as maintenance of joint homeostasis61 and, as a consequence, segmental homeostasis. It is dependent on a combination of muscle stiffness, inherent joint variables provided by the capsule, bony surfaces and ligaments, and the central nervous system (CNS).62,63 If the CNS interprets joint stability (homeostasis) to be at risk, movement pathways are likely to be adapted to protect the system by either inhibiting or facilitating different muscle groups.64 Stability provided by the active system depends not only on recruitment of the contractile components, but also on the viscoelastic properties of the tendons and the non-contractile connective tissue surrounding the muscle fibres.65 A critical muscle stiffness is defined as the minimal muscular stiffness required to stabilise the joint under a given load.66 Clinical observations and a number of the studies described above have shown that following injury, there is an inhibition or deloading of muscles with an anti-gravity and/or stabilising function, and facilitation of two-joint muscles, in particular the hamstring muscles.34,64 This pattern appears to be irrespective of the symptomatic area, e.g. lumbo-pelvic area or lower limb joints. In patients with low back or pelvic pain, decreased activity of the transverse abdominis, mulitifidi and gluteal muscles has been observed.28,67 Decreased and delayed activity of gluteus maximus in comparison to hamstring muscle activity during hip extension has also been found in subjects with a previous ankle sprain.68

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In addition to generating power, two-joint muscles can be used to fine tune movement.66,69,70 As a consequence, any threat to the stability of the lower limb and trunk could lead to increased demand on the hamstring muscle group in preparation of weight-acceptance. This would be most evident during the final swing phase in preparation for weight-acceptance and early stance phase to stabilise the leg – the phase of the running gait during which hamstring injuries appear to occur most commonly.71,72 Thus, it is possible that if the CNS perceives there is compromised stability of a joint or the whole body during walking or running, preactivation of muscles during the final swing phase could be altered in advance to protect the neuromusculoskeletal structures during load acceptance and impact absorption of ground contact. Such increased loading of the hamstring muscles during functional activity may lead to neuromuscular changes. Timedependent cumulative loading may result in changes in viscoelastic properties with decreased tissue strength, similar to suggestions regarding low back disorders,73 thereby increasing injury risk. The concept of increased activation of the hamstrings could help to explain strains occurring during sub-maximal activities and the symptoms of tightness, feeling of cramping and discomfort (Right arm of Fig. 1). Owing to increased recruitment, the threshold of injury would be reached sooner and the experience of pain or pulling sensation, as often described by the athletes, would likely occur during accustomed, sub-maximal activity.

Current concepts of hamstring injuries Strategies of prevention and management of hamstring injuries have focused mainly on concepts of muscle strength, flexibility, endurance and fatigue.1 Decreased muscle strength is often found in subjects with past hamstring injuries,74,75 and is considered a risk factor for injury.22 The decreased strength is most commonly proposed to be due to loss of structural integrity following musculotendinous tissue damage.76 In addition to structural damage, protective inhibition contributes towards apparent strength loss following an injury.77 Thus loss of strength, as measured by maximal strength tests, is likely to be due to a combination of pain inhibition (neurophysiological component), fear of pain (emotional component) and intrinsic tissue damage (structural component). The traditional concepts of prevention and management of hamstring injury based mainly on power

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Figure 1 Proposed mechanisms of (1) decreased tissue strength and (2) increased cumulative load contributing to the risk of injury of hamstring muscle

generation, maximal strength and flexibility may explain damage when this occurs at a maximal effort, such as sprinting (left arm of Fig. 1). However, injuries often occur during sub-maximal activities, in which case the aetiology may not be fully explained by loss of structural strength. In those athletes where the pain persists or recurs despite optimal rehabilitation or where a lesion is not visible with MRI, symptoms are often experienced and limit performance at sub-maximal levels.78 Magnetic resonance imaging findings have not been able to predict recurrence of injury,79 thus factors other than gross structural damage need to be considered for the aetiology of recurrence. In summary, although the function of the hamstring muscles has been historically described as a power generator and controller of knee extension during the swing phase of gait, its role towards controlling dynamic stability of the kinetic chain also needs to be considered. The authors hypothesise that loss of stability of any joint in the lower extremity and lumbopelvic area, irrespective of the underlying pathology or medical diagnosis, and possibly in combination with extrinsic factors, will increase the load of the hamstring muscle group (Fig. 1). Increased ‘base’ activation or cumulative loading could theoretically decrease the pain- and injury-free

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window of movement and activity before thresholds are reached. Such altered activation may be a substantial contributing factor towards development of a first or recurrent hamstring injury, as well as persistence of symptoms and decreased training levels following an injury. It is possible that in the early healing phases of a hamstring muscle injury or with a premature return to sports training and activity, recruitment of this muscle during functional movement is decreased or inhibited. Its stabilising function towards the knee and/or lumbopelvic segment could thereby be impaired. Consequently, a vicious cycle could develop leading to lumbopelvic, groin or knee pain and injuries. Further research is needed to confirm whether alterations in muscle recruitment patterns are associated with hamstring injuries and to determine relevant clinical assessment procedures. Electromyographic investigations may contribute towards the understanding of the effect of trunk stabilisation programmes in the management of acute and recurrent hamstring injuries.

Alternate rehabilitation strategies: emerging concepts If loss of stability is a contributing factor towards the aetiology of hamstring injury, this should be considered

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in the implementation of prevention and rehabilitation programmes. Only sub-maximal muscle contraction is needed to stabilise a segment, thus strengthening exercises may not affect impairment of the stabilising function.73 Instead of prescribing rehabilitative exercises with the aim of strengthening the muscle, it may be more appropriate to decrease the load on the muscle. A multi-structural approach to the prevention and treatment of hamstring injuries has been suggested recently and a concept based on stability would support such an approach.80,81 It has been shown in a small clinical trial that rehabilitation programmes that include trunk stability exercises are more successful in decreasing risk of recurrence, than those concentrating mainly on strengthening of the hamstring muscle group.13 Facilitation and rehabilitation of stabilising muscles, such as transversus abdominis and gluteus maximus, may lead to decreased loading of the hamstring muscle group. Programmes incorporating trunk control, particularly in weight-bearing and function-specific positions, should thus be considered.82 Currently, it is difficult to determine whether loss of SIJ stability contributes towards a hamstring injury. Manual therapy examination techniques of this joint are directed towards establishing whether this joint is a source of symptoms.83 Clinically, the authors have used extrinsic means of improving stability, firstly by considering the use of a pelvic belt as an adjunct to assessment and rehabilitative exercises, and second, by assessing footwear. The authors have found that in selected patients with hamstring injury, pain was decreased during bridging in the supine position (Fig. 2) while wearing a pelvic belt. Symptom decrease while wearing the belt is considered as an indicator of potential underlying loss of pelvic stability contributing towards symptoms. Similar reasoning has been used in the application of a pelvic belt or through manual compression across the pelvis by the therapist in recent studies of subjects with groin45 and sacro-iliac joint pain.84,85 Based on findings during clinical assessment, a pelvic belt may be used as a temporary measure with an aim of improving lumbopelvic stability, and possibly decreasing the critical muscle stiffness of the hamstring muscle. The authors recommend that, if required, such a belt is worn during rehabilitative exercises and also during daily activities, depending on the severity of symptoms. As symptoms reduce and training levels progress, the belt is used less frequently.

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Figure 2 Bridging on the symptomatic leg with a pelvic belt (arrow) applied. If symptoms decrease while wearing the belt, loss of pelvic stability may be contributing towards the symptoms

In patients with pelvic pain, the severity of the pain and impairment of muscle activation has been shown to decrease while wearing a pelvic belt85 or with manual compression across the pelvis.84 In a recent study, the effect of applying a pelvic belt on isometric hip adduction strength and ASLR in the supine position was investigated in athletes with groin pain.45 Weakness of the ASLR and of hip adduction improved significantly in a sub-group of these athletes while wearing the belt. Sacro-iliac joint stiffness, as demonstrated with colour Doppler investigations, has been shown to increase in asymptomatic subjects and in subjects with pregnancyrelated pelvic pain while wearing a belt.86,87 The belt may thus have a comparable function with respect to SIJ stiffness as that argued for transverses abdominis, gluteus maximus and hamstring muscle. Research pertaining to the effect of footwear on hamstring activity is lacking, although preliminary findings from one study suggest that an ‘antipronation orthotic’ increases hamstring activity before heelstrike in some subjects.59 If anti-pronation footwear increases hamstring activity levels, then shoes with wear or density changes of the lateral outer sole may have similar effects. Comfort of orthotics has been found to be associated with kinetic, kinematic and EMG variables during overground running in uninjured runners.88 Thus, in the absence of further research findings, comfort can potentially be used in the clinical setting to determine optimal footwear. It has been recommended that, in general, a ‘neutral’ shoe model with a stable hind-foot and flexible forefoot should be prescribed for sportspeople.89 More research is needed to investigate whether footwear plays a role in the aetiology of injury of this muscle. The authors thus propose that issues of stability should be considered in the prevention and management

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of hamstring injuries. More valid and sensitive clinical assessment procedures for testing stability need to be established, particularly pertaining to the lumbopelvic segment in functional positions. If loss of dynamic stability of the knee or the lumbopelvic area is a contributing factor towards an injury or an apparent hamstring weakness, hamstring muscle strength should improve with measures to optimise stability. However, comparative residual strength losses may also need to be addressed with appropriate resistance exercises.

Conclusion The function of the hamstring muscle group appears to be more complex than the literature has classically described. Factors other than strength, endurance and flexibility may need to be considered to fully understand the function of this muscle group and the effect that an injury has on its function. A stabilising role, described as increasing the stiffness of the SIJ, hip and the knee joint during weight acceptance of stance, may need to be considered. Furthermore, when considering physiotherapy treatment, the effect of these interventions on the stabilising function may need to be investigated. Such research will add towards a greater understanding of the high recurrence rate of this muscle group.

References 1

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GISELA SOLE University of Otago, Box 56, Dunedin, New Zealand Email: [email protected]

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