Evaluation and Management of Hamstring Injuries

The American Journal of Sports Medicine
http://ajs.sagepub.com/ Evaluation and Management of Hamstring Injuries

Christopher S. Ahmad, Lauren H. Redler, Michael G. Ciccotti, Nicola Maffulli, Umile Giuseppe Longo and James Bradley Am J Sports Med 2013 41: 2933 originally published online May 23, 2013 DOI: 10.1177/0363546513487063 The online version of this article can be found at: http://ajs.sagepub.com/content/41/12/2933
Published by:
http://www.sagepublications.com
On behalf of:
American Orthopaedic Society for Sports Medicine
Additional services and information for The American Journal of Sports Medicine can be found at: Email Alerts: http://ajs.sagepub.com/cgi/alerts Subscriptions: http://ajs.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> Version of Record - Nov 27, 2013 OnlineFirst Version of Record - May 23, 2013 What is This?
Downloaded from ajs.sagepub.com at Tel Aviv University on December 16, 2013
Clinical Sports Medicine Update
Evaluation and Management of Hamstring Injuries
Christopher S. Ahmad,* MD, Lauren H. Redler,*y MD, Michael G. Ciccotti,z MD, Nicola Maffulli, MD, Umile Giuseppe Longo,|| MD, and James Bradley,{ MD Investigation performed at the Center for Shoulder, Elbow, and Sports Medicine, Department of Orthopaedic Surgery, Columbia University, New York, New York
Muscle injuries are the most common injuries in sports, with hamstring injuries accounting for 29% of all injuries in athletes. These injuries lead to prolonged impairment and have a reinjury risk of 12% to 31%. They range from mild muscle damage without loss of structural integrity to complete muscle tearing with fiber disruption. Novel MRI scores are increasingly being used and allow a more precise prediction of return to sport. In this article, the authors review the history, mechanisms of injury, and classification systems for hamstring injuries as well as present the latest evidence related to the management of hamstring injuries, including intramuscular and both proximal and distal insertional injuries. Indications for surgical treatment of certain proximal and distal avulsions, biological augmentation to the nonoperative treatment of midsubstance injuries, and advances in risk reduction and injury prevention are discussed. Keywords: hamstring; biceps femoris; semimembranosus; semitendinosus; platelet-rich plasma; cell therapy; hamstring injury prevention; proximal hamstring repair; distal hamstring resection
Hamstring injuries are among the most common lower extremity injuries in athletes,3,32,34,57,132 accounting for up to 29% of all injuries in various sports21,40,57,99,100,128; in addition, they may produce prolonged impairment and an immense reinjury risk of 12% to 31%.40,48,128 These injuries are most common in sports requiring rapid acceleration such as running, hurdling, jumping, and kicking sports. Hamstring strains account for 50% of muscle injuries in sprinters and are the most common injury in hurdling.22 Most hamstring strains in the United States National Football League (NFL) are sustained during noncontact activities, with sprinting as the primary activity.48 Speed positions (receivers, defensive backs, and running backs) have significantly higher rates of hamstring muscle strains compared with strength positions (offensive and defensive linemen). Sports with ballistic movements such
Address correspondence to Lauren H. Redler, Center for Shoulder, Elbow, and Sports Medicine, Department of Orthopaedic Surgery, Columbia University, 622 West 168th Street, PH-11 Center, New York, NY 10032 (e-mail: lauren.redler@gmail.com). *Center for Shoulder, Elbow, and Sports Medicine, Department of Orthopaedic Surgery, Columbia University, New York, New York. z Center for Sports Medicine, Rothman Institute, Department of Orthopaedic Surgery, Thomas Jefferson University, Philadelphia, Pennsylvania. Centre for Sports and Exercise Medicine, Queen Mary University, London, United Kingdom. || Department of Trauma and Orthopaedics, Campus Biomedico University, Rome, Italy. { Center for Sports Medicine, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania. The authors declared that they have no conflicts of interest in the authorship and publication of this contribution. The American Journal of Sports Medicine, Vol. 41, No. 12 DOI: 10.1177/0363546513487063 2013 The Author(s)
y
as skiing, dancing, skating, and weight lifting are associated with hamstring injuries, particularly the proximal avulsion type.3,34 The injuries range from mild muscle damage without loss of structural integrity to complete muscle tearing with fiber disruption. Reductions in the incidence, severity, and reinjury risk of hamstring injuries have obvious potential to reduce medical costs and time lost from sport. Advances in diagnosis, classification, newer surgical and biological treatments, as well as prevention strategies may offer future benefits.
THE HAMSTRING MUSCLE GROUP Gross Anatomy

The hamstring muscle group consists of the biceps femoris (long and short heads), the semitendinosus, and the semimembranosus. All 3 muscles, except for the short head of the biceps femoris, originate from the ischial tuberosity as a common tendon. They then separate 5 to 10 cm distal to the ischium, with the semimembranosus first to become distinct.58 The muscle fibers of the biceps femoris are visible 6 cm distal to the tuberosity, and the proximal myotendinous junction encompasses approximately 60% of the total length of the muscle.58 The semimembranosus muscle fibers appear within the proximal 30% of this muscle, and the semitendinosus muscle fibers insert directly to the ischial tuberosity at the proximal musculotendinous junction.58 The short head of the biceps femoris originates just medial to the linea aspera in the posterior distal femur. The long head of the biceps femoris attaches to the fibular head and the lateral tibia.120 The short head
2933
2934 Ahmad et al
of the biceps femoris attaches into the tendon of the long head of the biceps femoris as well as fascial and tendinous insertions to the posterolateral capsule, the iliotibial tract, the fibular head, and the proximal lateral tibia.120 The semimembranosus has multiple insertions at the posteromedial corner of the knee.124 The semitendinosus joins the sartorius and gracilis tendons to form the pes anserinus on the medial aspect of the proximal tibia, overlying the medial collateral ligament. The distal musculotendinous complex covers approximately 66% of the length of the biceps femoris and slightly more than 50% of the length of the semimembranosus and semitendinosus muscles.124 The semimembranosus, semitendinosus, and long head of the biceps femoris are innervated by the tibial portion of the sciatic nerve, and the short head of the biceps is innervated by the peroneal portion of the sciatic nerve. The semimembranosus adds stability to the knee and functions to flex and medially rotate the leg at the knee as well as extending, adducting, and medially rotating the thigh at the hip.2,32,88 The semitendinosus is a flexor and internal rotator of the tibia at the knee and also provides valgus stability to the knee.2,32,88 The short head of the biceps functions to flex the knee with the thigh extended; the long head gives posterior stability to the pelvis and extends the femur at the hip.2,32,88
degradation, and inflammation. Blood vessel damage results in bleeding and clotting. A local ischemic environment can result, causing further muscle damage and edema. The healing process involves muscle regeneration and fibrosis. A properly aligned extracellular matrix is required to maintain optimal myofibril orientation. With an intact or repaired basal lamina acting as a scaffold, myofibrils can regenerate. Early range of motion after injury can minimize disorganized scar formation and reinjury.116
Risk Factors for Injury

A variety of risk factors have been proposed for hamstring injuries, including inadequate warm-up, strength imbalance, lower extremity flexibility,17,63,126 core stability,38,64,90,112 muscle weakness,41,42,99 fatigue,87,128,132 dehydration, and a history of injury.8,13,49,55,101 Strength imbalance refers to either a difference in hamstring strength between lower extremities or an altered ratio of hamstring-to-quadriceps strength in the same extremity.32,77,129 Thresholds of side-to-side hamstring deficits of .10% to 15% or a hamstring-to-quadriceps strength ratio of \0.6 increase the injury risk.24,32,71,77 These ratios, however, most likely vary with sex, sport, and position played.** Muscle weakness40,42,118,131 and, more recently, poor core stability have been associated with hamstring injuries.31,64,90,112 Lumbopelvic position, which is in part controlled by abdominal muscle activity, may influence hamstring muscle length and stiffness.31,73 Fatigue is a risk factor, and more hamstring injuries occur toward the end of an athletic competition.47,128 Animal studies have demonstrated that eccentric loads of fatigued muscles result in significantly more damage than isometric or concentric loads.46,104 Similarly, increasing muscle temperature may increase the ability of the muscle tendon unit to absorb force.46,104 Flexibility remains controversial as a risk factor. Prospective studies8,13,49,55,56,99,131 demonstrate no relationship between flexibility of the knee flexors and hamstring injury, but other studies have shown an association between flexibility values obtained in preseason training and injuries suffered during the season.17,63,126,129,130 In addition, an association between reduced hip flexor flexibility and the risk of hamstring injuries has been reported.54 Seasonal timing of hamstring strains has been demonstrated in the NFL, with the preseason identified as the most vulnerable period.48 Factors implicated in this trend are the relative deconditioning and muscle weakness that occur in the off-season. Perhaps the most significant risk factor is a previous hamstring injury, which increases the risk of reinjury by 2 to 6 times.7,13,49,55,101 A previous hamstring injury may lead to the formation of weakened scar tissue at the injury site, thereby lowering the threshold to a recurrent injury.3,21,49,51,56,123
**
Mechanism of Injury
The hamstring muscle group spans both the hip and knee joints, producing potential for rapid and extreme muscle lengthening. Injury occurs most commonly during eccentric muscle contraction.57,132 During the last 25% of the swing phase, the hamstrings assist in proximal hip extension while decelerating knee extension distally. The hamstrings remain active during the first half of the stance phase to produce hip extension and resist knee extension through a concentric contraction.2 Sprint mechanics research suggests that strain injury risk is greatest near the end of the swing phase, when the hamstrings reach maximal length and undergo eccentric contraction just before heel strike.61,108 The mechanism of proximal avulsions is through an eccentric contraction with the hip flexed and the knee extended and occurs with higher energy ballistic activities.#
Pathological Changes
The myotendinous junction experiences the highest eccentric loads and is the most common location of injury.32,34,36,38,89 Muscle belly injuries are less common but can occur with direct trauma or contusion.3,32 Complete ruptures are rare and tend to occur with pre-existing tendinopathy. In the simplest injury, only the myofibrils are damaged, resulting in leakage of the cytoplasmic enzyme creatine kinase. With greater injury severity, the extracellular matrix and fascia become damaged, followed by release of muscle enzymes, collagen and proteoglycan
#
References 22, 32, 34, 66, 88, 106, 107, 127, 132.
References 2, 19, 24, 25, 32, 40, 62, 71, 88, 104, 132.
Vol. 41, No. 12, 2013
Hamstring Injuries 2935
Figure 2. The Puranen-Orava test for hamstring tendinopathy and strain. more commonly, distal avulsion, a thickened area of subcutaneous tissue may be identified adjacent to the injury.34,36,38 Palpation of the injured posterior thigh from the ischial tuberosity to the posterior aspect of the knee localizes the injury by eliciting either tenderness or appreciating a defect. Precise location is often difficult, given the deep location of the muscles, especially proximally. The range of motion of both lower extremities should be assessed. A careful comparison of side-to-side symmetry of the hips and knees will help to estimate the severity of the injury. The popliteal angle is determined by flexing the hip to 90 with the knee flexed to 90 and then slowly extending the knee passively. The knee flexion angle at which posterior thigh pain and guarding occur is compared with that in the contralateral, uninjured leg. An increased angle on the affected side suggests a hamstring injury.32 Hamstring strength should then be assessed with the patient in the prone position and the knee flexed to 90. Resisted active knee flexion may help to more precisely determine the location and severity of the injury. Active knee flexion while the examiner extends the knee to 30 reproduces the common eccentric load mechanism and also aids in diagnosis. These maneuvers should be compared with the uninjured limb. Several special provocation tests have more recently been proposed to evaluate hamstring injuries, particularly tendinopathy and milder strains.26 The Puranen-Orava test (Figure 2) is performed by an active stretch of the hamstrings with the patient standing. The hip is flexed to 90; the knee is then fully actively extended, and the heel is held on a support. The bent-knee stretch test (Figure 3) is performed with the patient supine. The hip and knee of the symptomatic extremity are maximally flexed, and the knee is then slowly passively extended by the examiner. The modified bent-knee stretch test (Figure 4) is also performed with the patient supine and the symptomatic leg fully extended. The examiner maximally flexes the hip and knee and then rapidly extends the knee. With
Figure 1. Clinical appearance of diffuse posterior thigh ecchymosis with a proximal myotendinous hamstring injury.
Clinical Presentation
History. Most athletes experience acute, sudden sharp pain in the posterior thigh, often with an audible or palpable pop,32,129 during an activity requiring a combination of sudden hip flexion and knee extension as in running, jumping, and kicking sports.3,32,129 A smaller number note an insidious onset of progressive hamstring tightness,38,129 and some athletes may have an acute or chronic onset.32,129 Some athletes experience loss of hamstring flexibility, particularly with recurrent mild episodes of injury. Proximal avulsion injuries may cause discomfort with sitting. Athletes often describe difficulty in walking smoothly. Physical Examination. Inspection begins with an assessment of gait with a stiff-legged gait pattern often noted as the athlete attempts to avoid simultaneous hip flexion and knee extension.3,34 Most often, minimal ecchymosis is observed; however, broad ecchymosis along the posterior thigh may be encountered and may indicate a high-grade myotendinous injury or a proximal avulsion injury (Figure 1). In cases of a muscle belly rupture, a defect may be palpable.32 With either proximal or,
2936 Ahmad et al
Figure 3. Bent-knee stretch test for hamstring tendinopathy and strain.
Figure 4. Modified bent-knee stretch test for hamstring tendinopathy and strain. respect to all 3 tests, hamstring tendinopathy or strain is indicated by increasing posterior thigh pain with extension of the knee. All 3 tests have been shown to have moderate to high validity and reliability in identifying hamstring tendinopathy and strains.26 Finally, it is important to perform a thorough neurovascular examination; peroneal nerve
Vol. 41, No. 12, 2013
Figure 5. Plain radiograph of the pelvis, demonstrating an avulsion injury from the ischial tuberosity.
Figure 7. Proximal hamstring (semimembranosus) avulsion injury with retraction on coronal T2-weighted magnetic resonance imaging.
Figure 6. Longitudinal ultrasound image of a proximal myotendinous hamstring injury. A high-grade tear is identified by the large white arrow, intact muscle is indicated by arrowheads, and the tendon origin (*) is seen at the ischial tuberosity (Tub).
injury, while usually a neurapraxia and self-limiting, can result in subtle foot drop or eversion weakness. The differential diagnosis for hamstring injuries includes a variety of lesions occurring proximally at the hip and pelvis, along the posterior thigh, or distally at the knee. Proximal injuries include ischial tuberosity apophysitis, painful unfused apophysis, piriformis syndrome, gluteus medius insertional tendinopathy, posterior trochanteric bursitis, sacroiliitis, pelvic stress fracture, and lumbar radiculopathy. Posterior thigh injuries include iliotibial band syndrome, lumbar radiculopathy, and sciatica. Distal injuries include knee capsular strain, knee collateral ligament sprain, knee meniscal injury, lumbar radiculopathy, gastrocnemius strain, popliteal cyst formation or rupture, and pes anserine bursitis. Imaging. Plain radiographic findings of the pelvis, hip, femur, and knee are most often negative in athletes with hamstring injuries,3,32,34 unless an avulsion fracture has occurred from the ischial tuberosity (Figure 5). Dynamic ultrasonography provides high-resolution imaging with
Figure 8. Cross-sectional muscle involvement on axial T2weighted magnetic resonance imaging.
the advantages of direct correlation with physical examination and perhaps access to more immediate imaging from portable ultrasound machines. Typically, hamstring muscles and tendons are imaged using a linear probe in both the longitudinal and transverse planes with
2938 Ahmad et al
Figure 9. (A) Proximal myotendinous hamstring injury on coronal T2-weighted magnetic resonance imaging (MRI). (B) Muscle belly injury on axial T2-weighted MRI. (C) Distal avulsion hamstring injury on coronal T2-weighted MRI. TABLE 1 Magnetic Resonance Imaging Scoring System for Hamstring Injuries
Points 0 1 2 3 Age, y No. of Muscles Involved Location Insertion Involvement No 25 26-31 32 1 2 3 Proximal Middle Distal Yes Cross-sectional Injury, % 0 25 50 75 Retraction, cm None \2 2 Long-Axis T2 Length, cm 0 1-5 6-10 .10
frequencies in the 7.5- to 13-MHz range.3,89 Higher frequencies provide better resolution, while lower frequencies provide better penetration. Ultrasound demonstrates fluid collections around and along the injured muscle and depicts areas of echogenicity, representing edema and/or hemorrhage (Figure 6). Ultrasonography is extremely accurate in the acute phase to determine the location and extent of a hamstring injury.3,89 Magnetic resonance imaging (MRI), however, is the most commonly used imaging study to evaluate hamstring injuries. Standard axial, coronal, and sagittal T1- and T2-weighted images are obtained on a 1.5-T or higher unit. For proximal hamstring injuries, images are obtained through both ischial tuberosities and proximal thighs; for distal injuries, images are obtained from the midthigh through the knee. Higher resolution images are then obtained through the injured thigh. Also, MRI precisely defines the injury location, degree of damage, number of involved tendons, extent of retraction, and chronicityyy (Figures 7 and 8). With respect to location, MRI can precisely identify the injury site from the origin, proximal myotendinous junction, muscle belly, distal junction, or insertion (Figure 9). Moreover, MRI can determine the degree of soft tissue damage by defining (1) dimensions of abnormal intramuscular and extramuscular T2 hyperintensity, (2) percentage of abnormal crosssectional muscle area, (3) percentage of abnormal muscle volume, and (4) length of extramuscular T2 signaling113;
yy
MRI can also determine the chronicity of injury as indicated by fibrosis.38 Further, MRI better defines a bone injury seen with proximal or distal avulsions as well as more delayed soft tissue changes seen with more chronic injuries and can assess progressive healing.18,37,89
CLASSIFICATION
Hamstring injuries have traditionally been classified with respect to their clinical presentation: (1) grade 1 (mild) as characterized by overstretching but minimal loss of the structural integrity of the muscle-tendon unit, (2) grade 2 (moderate) as having partial or incomplete tearing, and (3) grade 3 (severe) as a complete rupture.32,132 The generally accepted MRI grading system for muscle injury includes (1) grade 1 as defined by a T2 hyperintense signal about a tendon or muscle without fiber disruption, (2) grade 2 as represented by a T2 hyperintense signal around and within a tendon/muscle with fiber disruption less than half the tendon/muscle width, and (3) grade 3 as defined by tendon/muscle disruption less than half its width.111 Alternatively, hamstring injuries can be classified based on the anatomic site, pattern, and severity of the injury in the acute stage, as assessed by MRI or ultrasound.30 Important to the management of hamstring strains is the early determination of time required to return to full competition. Neither the traditional clinical nor the general MRI classifications have been precisely correlated
References 3, 18, 32, 34, 36, 45, 89, 111, 113.
Vol. 41, No. 12, 2013
with time to return to play after a hamstring injury. Several authors have attempted to assess the predictive value of MRI for return to play in athletes with these injuries.10,18,36,113,122 Verrall et al122 evaluated 83 elite Australian rules football players with clinically diagnosed hamstring strains and observed that those athletes who had MRI features of a hamstring injury averaged 27 days missed from competition and those with no changes on MRI missed an average of 16 days. Askling et al10 prospectively evaluated 18 elite sprinters with clinically diagnosed hamstring strains and serial MRI evaluations at 10, 21, and 42 days after injury. Proximal injuries demonstrated a prolonged time to return to play. Verall et al123 used MRI to assess the volume and percentage of muscle injury and found it was predictive of time lost from competition. Slavotinek et al113 also noted that the percentage of abnormal muscle area and the volume of injury correlated most precisely with time to return to sport, but no classification was proposed. Cohen et al36 have provided the most detailed MRI classification system that correlates the extent of hamstring injury with time to return to play. These authors evaluated 38 NFL players with acute hamstring strains. Their MRI scans were evaluated with the traditional radiological muscle injury grading system as well as a new MRI scoring system. This scoring system (Table 1) was based on (1) player age, (2) number of muscles involved, (3) location of injury, (4) presence of insertional damage, (5) percentage of cross-sectional muscle involvement, (6) length of muscle retraction, (7) long-axis T2 sagittal plane signal abnormalities, and (8) presence of chronic changes. All scores were then correlated with time missed from competition. These authors noted that rapid return to play (\1 week) correlated with isolated injury of the long head of the biceps femoris, \50% cross-sectional involvement, and minimal perimuscular edema (grade 1 traditional radiological strain) and an MRI score of \10. Prolonged recovery (.2-3 weeks) correlated with multiple-muscle injury, injuries distal to the myotendinous junction, short head of the biceps injury, .75% cross-sectional involvement, presence of retraction, circumferential edema (grade 3 traditional radiological strain), and an MRI score of .15. These authors suggested that this novel MRI score is highly predictive of time missed from competition. Additional future systematic studies for different sports will be important for the validation of this MRI score in predicting return to play for other athletes.
Treatment: Noninsertional Injuries

Initial nonoperative treatment includes activity modification, ice, compression, stretching, early physical therapy, and nonsteroidal anti-inflammatory drugs (NSAIDs) with sport-specific activity progression carried out with attention to the athletes symptoms. Other modalities include massage, ultrasound, and electrical stimulation. A recent randomized controlled trial showed shockwave therapy to be safe, effective, and superior to traditional modalities in professional athletes with proximal hamstring
tendinopathies.27 Intramuscular corticosteroid injection has also been advocated as an early treatment to prevent prolonged disability.65,75 Potential risks include infection, subsequent tendon rupture, increased likelihood of a recurrent hamstring injury, postinjection pain flare, subcutaneous fat atrophy, and skin hypopigmentation.98 The proposed beneficial mechanism is mediation of the painful inflammatory response triggered by the acute muscle strain. In the NFL, in players with severe discrete injuries within the substance of the muscle, intramuscular corticosteroid injection decreased time to return to full play without a risk of further injuries or complications.75 Traditional management has been disappointing, with unpredictable time lost, high reinjury rates, and poor restoration of preinjury status. New biological therapies are therefore being investigated, including platelet-rich plasma (PRP) treatment, cell therapy, tissue engineering, and administration of growth factors.81 Bioactive molecules include transforming growth factorb (TGF-b), fibroblast growth factor (FGF), epidermal growth factor (EGF), platelet-derived growth factor (PDGF), and vascular endothelial growth factor (VEGF). These play a crucial role in the repair process of injured skeletal muscle, including hamstring strains, namely by stimulating myogenesis65 and neoangiogenesis.68 Thus, they represent a potential therapeutic option in improving the healing process. Platelet-Rich Plasma. Platelet-rich plasma is a concentrated source of autologous platelets and the growth factors that their a granules naturally contain. Given these bioactive molecules, PRP has the potential to improve the healing process, and thus, its use has been proposed for the management of many musculoskeletal injuries, including hamstring strains.59,125 Although its efficacy has not been proven, PRP has been widely described in the orthopaedic literature because of its ease of acquisition and safety.6,53 Mejia and Bradley93 reported on their experience with autologous conditioned plasma injections within 24 to 48 hours for acute hamstring injuries in NFL players. Their results show an earlier return to play of 3 days for grade 1 and 5 days for grade 2 injuries, with an overall 1-game difference in the return to play. Most encouragingly, the authors noted a 0% recurrence rate compared with their baseline of 2 to 4 recurrences per year. Despite promising results from level IV studies, as well as several basic science and animal studies that suggest PRP can enhance healing,5 there are no level I studies with adequate outcome measures and follow-up assessment that prove its superiority. Several devices and systems are available for PRP preparation, with varying concentrations of growth factors, making comparisons between clinical studies difficult. Additionally, there is concern that, if excessive quantities of PRP are used, it may induce a florid fibrotic healing response in muscle tissues by increasing the local concentration of TGF, based on data that TGF seems to be able to induce fibrosis in cultured muscle tissue.65 Therefore, at present, there is no evidence to recommend or discourage the adoption of PRP in clinical practice. Further research is required to standardize formulations (number of platelets and/or leukocytes) and administration regimens, including volume of injection
2940 Ahmad et al
and timing of treatment, to optimize PRP application for the management of muscle injuries. Cell Therapy. Regenerative medicine involving tissue engineering and cell therapy has been directed toward skeletal muscle.1,14,33 Stem cells directly participate in tissue regeneration and thus influence muscle healing.39,76,82 After injury, patterns of growth factor expression determine which cell types will participate in the wound healing process.76 High levels of TGF-b3 are related to the activation of mesenchymal progenitor cells derived from traumatized muscle to promote wound healing after muscle injury.67 On the other hand, high levels of TGF-b1 lead to muscle fibrosis by activating fibroblasts.39,82 Animal models of muscle injury have shown that muscle-derived stem cells (MDSCs) improve both muscular structure11,28,121 and muscle regeneration.12 Two potential techniques for skeletal muscle tissue engineering are in vitro and in vivo. With in vitro tissue engineering, stem cells from adult skeletal muscle are expanded and seeded on a 3-dimensional (3D) scaffold. After the differentiation of stem cells, the neotissue graft could be transplanted in the injured region. With in vivo tissue engineering, the isolated MDSCs are seeded on a 3D scaffold carrier and immediately transplanted, obtaining direct delivery of stem cells in the muscle lesion.103 At this time, the clinical use of stem cells is limited. Further research is necessary to identify the mechanisms involved in muscle regeneration to exactly understand the therapeutic potential of stem cells. Recurrence and Prevention. Prevention of hamstring injuries is essential. Eccentric exercise is now emphasized and produces greater strength gains than similar concentric hamstring movements.7,20,69,97 Improved hamstring strength and endurance in a more functional position during sprinting increase the ability of the hamstrings to absorb repeated eccentric loads before and during heel strike. Identifying and correcting muscle imbalance and optimizing neural timing along with progressive sprint training for identified high-risk athletes are advocated.48,87 Prevention strategies are likely most beneficial as part of a preseason training program. Athletes are encouraged to follow prevention programs and may comply because the programs are closely associated with overall athletic performance.9,57 A few studies have investigated the effect of injury prevention programs on altering proposed risk factors for lower extremity injury.74,78 The injury prevention program de ration The 11, developed with the support of the Fe Internationale de Football Association (FIFA), aims to reduce the effect of intrinsic injury risk factors in soccer, and it has been validated in that sport.117,119 A successive modified version of The 11 (The 111) has been also shown to be effective in preventing injuries in young female soccer players114 and elite male basketball players.80 The 111 provided more than a 40% reduction in injury risk.114 Unfortunately, the program was not effective in preventing the following injuries: ankle, anterior thigh, posterior thigh (hamstrings), hip/groin, sprains, strains, fractures, or anterior lower leg pain (periostitis).
On the other hand, the program was effective in preventing knee injuries, lower extremity injuries, overall injuries, severe injuries, and overuse injuries, such as lower extremity tendon pain and low back pain. Therefore, the effectiveness of hamstring injury prevention programs remains controversial and deserves more attention.83-86
Treatment: Proximal Insertional Injuries

Essential to the treatment of proximal hamstring injuries is the early recognition of the injury and timely referral to proper specialists. In general, nonoperative treatment is considered for proximal hamstring injuries that involve a single tendon and/or multiple-tendon injuries with \2 cm of retraction. However, patient factors such as noncompliance, age, and activity level may influence treatment. Surgical indications for proximal hamstring injuries include those involving 2 tendons with .2 cm of retraction and 3-tendon tears. Identification and treatment of surgical proximal hamstring injuries are best managed within 4 weeks, as later recognition provides for a more difficult repair, leading to increased surgical complications and possibly inferior outcomes.35 Nonoperative Treatment. Single-tendon avulsions and 2tendon tears with retraction \2 cm are treated nonoperatively.34 Less active patients, those with medical comorbidities, and patients unable to comply with postoperative rehabilitation are also indications to manage these injuries nonoperatively. Nonoperative management consists of activity modification, NSAIDs, and physical therapy. Other rehabilitation modalities include ultrasound, shockwave therapy, electrical stimulation, and edema control.115 As the symptoms resolve, the core (abdominal), hip, and quadriceps may be added to a more aggressive program to prevent hamstring injuries.94 Pain can be a limiting factor in the progression of rehabilitation. If patients experience difficulty with reintegration programs, an ultrasound-guided corticosteroid injection can be used to provide initial relief in up to 50% of patients at 4 weeks.133 An alternative to corticosteroid injections includes PRP performed under computed tomography or ultrasound guidance, which has similar outcomes to corticosteroid in experienced hands. These injuries may take up to 6 weeks for initial healing. In single-tendon tears, 6 weeks allows the tendon time to fibrose to the intact tendons, often allowing the initiation of limited activity. However, full return to sport should only be allowed once the patient is asymptomatic with regard to pain and strength has returned to within 1 grade of the contralateral leg.95 In many tears managed nonoperatively, symptoms can persist beyond the normal healing times. Knee flexion weakness and hip extension weakness often ensue months after injury. Furthermore, a deformity in the area of the proximal hamstrings, difficulty in sitting, and scarring of the proximal hamstrings to the sciatic nerve can occur. A serious complication of nonoperatively treated proximal hamstring injuries is hamstring syndrome, characterized by local posterior buttock pain, discomfort over the ischial tuberosity during sitting, and worsening pain during stretching and exercises that target the hamstrings.43
Vol. 41, No. 12, 2013
Figure 10. Patient positioning for proximal hamstring repair. (A) Position of the table in slight flexion and (B) patient draping.
Figure 11. Transverse incision with optional longitudinal limb (dotted line) for proximal hamstring surgical approach. the gluteal fascia. The gluteus maximus muscle is next identified and is elevated superiorly, or a split in one of the septae overlying the ischial tuberosity can be performed to expose the hamstring fascia. Once the hamstring fascia is identified, a longitudinal incision is made through this fascia to locate the hamstring tendons. Often, these tendons are encased in scar tissue and erroneously appear to be intact. Care must be taken to excise the overlying scar tissue, uncover the underlying hematoma, and identify the injured hamstring tendons. The sciatic nerve is identified by palpation and can be protected by retracting the tendons laterally (Figure 12). The sciatic nerve is dissected free only in cases of chronic injury with possible sciatic nerve scarring or possibly in cases in which the patient presents with sciatic nerve symptoms preoperatively. The sciatic nerve is on average 1.2 cm lateral to the most lateral aspect of the ischial tuberosity.96 Once the sciatic nerve has been safely protected, another layer of fibrous tissue is often identified at the ends of each tendon. This fibrous tissue represents scarring of the tendons and should be partially removed to allow for adequate healing of the tendons after repair. However, overzealous removal of this tissue could prevent adequate mobilization of the proximal hamstrings and produce shortened tendons. Once the tendons are mobilized, they are tagged with heavy suture before identifying and preparing the ischial tuberosity for tendon reattachment. A periosteal elevator or a curette is used to clear off the lateral aspect of the ischial tuberosity to allow anatomic placement of the hamstring tendons (Figure 13). The tuberosity is then stimulated using manual instruments, allowing for a vascular bed for healing of the tendon origins to
These patients may benefit from surgical debridement and late repair. In cases of recalcitrant hamstring syndrome, the sciatic nerve should be managed with surgical neurolysis, which has an 88% success rate in some series.102 Operative Treatment. Operative treatment for proximal hamstring tendon avulsions is recommended when 2 tendons are retracted 2 cm or for 3-tendon avulsions.34 Two-tendon injuries may often involve injury to a third hamstring muscle, either at the muscle belly or the musculotendinous junction, that may not be seen on imaging studies that are focused on proximal hamstring insertions.34 This possible third hamstring injury should be taken into consideration when deciding between operative and nonoperative treatment in 2-tendon tears. Operative treatment has high success rates and is also a consideration for chronic injuries with complete or partial tears that fail nonoperative management.16,29,43,105,107,127 However, most studies indicated that the results of surgery for chronic ruptures are inferior to acute repair.60,92 Surgical Procedure. The procedure involves placing the patient prone on the operating room table with all bony prominences well padded and the trunk in slight flexion (Figure 10). A transverse incision is made at the gluteal crease directly inferior to the ischial tuberosity (Figure 11). Transverse incisions, in comparison to T-shaped or longitudinal incisions, allow improved cosmesis and accessibility to avulsed tendons that insert along the coronal plane.43,70 The incision is deepened through the subcutaneous fat to the gluteal fascia. Care must be taken to avoid the posterior femoral cutaneous nerve. Once this nervous structure is protected, a transverse incision is made in
2942 Ahmad et al
Figure 12. Identification of the sciatic nerve with lateral retraction.
Figure 14. X configuration of sutures on the ischial tuberosity. (A) Sutures through the tendon. (B) Final configuration.
Figure 13. Surgical field with the ischial tuberosity exposed. Yellow dotted line shows the lateral aspect of the ischial tuberosity. (A) Skin markings. (B) Surgical field.
the tuberosity. Motorized instruments are discouraged for this portion of the surgery, as they can risk nerve injury. Some authors recommend making longitudinal scales in the tuberosity using a small osteotome as a way to stimulate biological healing. Suture anchors (2.4-mm BioComposite SutureTak with No. 2 FiberWire, Arthrex Inc, Naples, Florida) are then placed in an X configuration to repair the tendons to bone with a total of 5 anchors (Figure 14). Special attention is paid to the anatomic location of the proximal hamstring tendons (Figure 15). The semimembranosus tendon is the most lateral structure, with the confluent semitendinosus and long head of the biceps appearing more medial. Regarding the footprint of the hamstring insertion, the semitendinosus and biceps femoris share an oval-shaped footprint 2.7 cm long from proximal to distal and 1.8 cm wide from medial to lateral.96 The semimembranosus footprint is crescent and lays lateral to the semitendinosus and biceps femoris footprint. It measures 3.1 cm from proximal to distal and 1.1 cm from medial to lateral.96 The sutures are placed through the tendon ends in a horizontal mattress pattern (from inferior to superior and tied down from superior to inferior). The knee is flexed to approximately 30, while the tendons are tied down. The
Figure 15. Insertion of hamstring tendons on the ischial tuberosity.
fascia is closed, and the wound is closed in layers. Using the above technique, a 96% satisfaction rate and .75% recovery of strength have been documented.35 Patients with chronic ruptures who require operative treatment may require an allograft bridge from the retracted tendon to the tuberosity. Reconstruction can be undertaken using an Achilles allograft with comparable results to acute surgical repair.50 Postoperative Rehabilitation. Postoperative rehabilitation is an essential part of this surgery. To limit stress at the surgery site, immediately after wound closure, the operative leg is placed in a custom-fitted orthotic for the hip that restricts flexion of the hip from 30 to 40 (Figure 16). Patients are prescribed aspirin for 4 weeks postoperatively for deep vein thrombosis (DVT) prophylaxis, although the risk of DVT after a hamstring injury has not been firmly established. The first 10 to 14 days involve toe-touch weightbearing with crutches. Weeks 2 to 5 consist of continued use of the hip orthotic and 25% weightbearing. Passive range of motion of the hip with
Vol. 41, No. 12, 2013
Figure 17. Axial magnetic resonance imaging scan demonstrating a distal semitendinosus tear. (A) Distally at the semitendinosus insertion (*), showing fluid signal intensity within the expected course of the tendon sheath (arrowhead), and (B) proximally at the retracted tendon stump (arrow).
Figure 16. Postoperative brace with the hip placed in 30 to 40 of flexion. a therapist begins at 2 weeks, and active range of motion begins at 4 weeks. At 6 weeks, the brace is discontinued, and the patient is allowed to fully bear weight and begin gait training along with isotonic exercises. Also at 6 weeks, aqua therapy is introduced along with isotonic exercises, core strengthening, and closed chain exercises; range of motion is increased with caution for extreme ranges. Dynamic training and isometric strengthening begin at 8 weeks after surgery, and at 10 weeks, an isometric strength evaluation is performed with the knee at 60 of flexion. Sport-specific training and dry land training begin at 12 weeks. A fully isokinetic evaluation is performed at 16 weeks at 60 deg/s, 120 deg/s, and 180 deg/s. These results are compared with the contralateral leg. Full return to sport is allowed once the operative leg is 80% of the nonoperative leg on isokinetic testing. Return to sport after operative treatment, with accomplishment of the above parameters, typically happens between 6 and 10 months.15 Complications. Early complications most commonly involve the sciatic nerve and include neurapraxia or stretch injury during surgery that eventually resolves. However, this can lead to burning pain radiating down the leg and weakness of the distal operative extremity immediately after surgery and in the first few weeks, making preoperative assessment of nerve symptoms essential. Other nerves that can be potentially harmed are the posterior femoral cutaneous nerve and the inferior gluteal nerve, leading to dysesthesia and weakness of hip extensors, respectively. Nonneurogenic complications include
those mentioned for the late sequelae of nonoperative treatment and comprise knee flexion weakness, hip extension weakness, and deformity. Superficial and deep infections can also occur and are a special concern for this surgery because of the location of the surgical site and its proximity to the gastrointestinal and genitourinary systems. Other complications include the risk of rerupture and loss of strength. Outcomes. Most series report that return of strength ranges from 60% to 90% of the contralateral leg, with more than 95% reporting good to excellent subjective results after surgical repair.15,23,29,43,70 In a series of 52 patients, Cohen et al35 showed that 98% of patients were satisfied with their outcome after surgery. Objective measures such as the Lower Extremity Functional Scale and custom Marx score showed a statistical difference between acute and chronic repairs, with acute repairs exhibiting improved outcomes. However, patient questionnaire averages did not show a statistical difference between acute and chronic repairs. This indicates that injuries with delayed diagnosis and failed nonoperative proximal hamstring injuries can still have favorable subjective patient outcomes when treated with operative repair.35
Treatment: Distal Insertional Injuries

The distal attachment of the biceps femoris is most commonly injured with a varus hyperextension mechanism as part of multiligament knee injuries.44,52,72,91 An isolated distal semimembranosus avulsion is rare.4 In contrast, isolated distal semitendinosus tendon avulsions are becoming more recognized38,109,110 but can be misdiagnosed as a distal-third muscle belly hamstring injury. An MRI scan of the thigh and knee over the full course of the semitendinosus tendon can confirm the diagnosis (Figure 17). Distal semitendinosus tendon avulsions cause much more time loss from sports than hamstring muscle belly injuries on average. Cooper and Conway38 reported a case series of 25 distal semitendinosus tendon ruptures in high-level athletes. Early treatment always involved nonoperative treatment, including rest, modalities, and rehabilitation
2944 Ahmad et al
exercises, followed by functional progression. Forty-two percent failed initial nonoperative treatment and subsequently had surgery with resection of the torn tendon and adjacent scar tissue, with an average recovery time of 12.8 weeks. Another group of patients were treated with acute surgery that resected the torn tendon and adjacent scar tissue within 4 weeks of injury. The acute-phase group had an average recovery of 6.8 weeks after surgery. The authors concluded that distal semitendinosus ruptures frequently do not recover when treated nonoperatively. Therefore, acute surgery may be considered in elite athletes for whom time to recovery is very important for more favorable time frames to return to participation. Further indications for immediate surgery are the presence of a painful mass, inability to walk well with a normal gait pattern, or inability to extend the knee fully.79
SUMMARY
Hamstring injuries occur in athletes of all ages, all types of sport, and all levels of competition. Most often, a detailed history, a thorough physical examination, and a complete review of the imaging studies will confirm the presence of a hamstring injury. Clinical grading, traditional radiographic grading, and a novel MRI scoring system may allow a more precise prediction of return to sport. Surgery is indicated for certain proximal and distal avulsion injuries. Nonoperative treatment of midsubstance injuries may include biological treatment in the future. Prevention strategies will also be beneficial. An online CME course associated with this article is available for 1 AMA PRA Category 1 CreditTM at http:// ajsm-cme.sagepub.com. In accordance with the standards of the Accreditation Council for Continuing Medical Education (ACCME), it is the policy of The American Orthopaedic Society for Sports Medicine that authors, editors, and planners disclose to the learners all financial relationships during the past 12 months with any commercial interest (A commercial interest is any entity producing, marketing, re-selling, or distributing health care goods or services consumed by, or used on, patients). Any and all disclosures are provided in the online journal CME area which is provided to all participants before they actually take the CME activity. In accordance with AOSSM policy, authors, editors, and planners participation in this educational activity will be predicated upon timely submission and review of AOSSM disclosure. Noncompliance will result in an author/editor or planner to be stricken from participating in this CME activity.
REFERENCES
1. Adams RD, Walton JN. The response of the normal, the denervated and the dystrophic muscle-cell to injury. J Pathol Bacteriol. 1956;72(1):273-298. 2. Agre JC. Hamstring injuries: proposed aetiological factors, prevention, and treatment. Sports Med. 1985;2(1):21-33.
3. Ali K, Leland JM. Hamstring strains and tears in the athlete. Clin Sports Med. 2012;31(2):263-272. 4. Alioto RJ, Browne JE, Barnthouse CD, Scott AR. Complete rupture of the distal semimembranosus complex in a professional athlete. Clin Orthop Relat Res. 1997;336:162-165. 5. Alsousou J, Thompson M, Hulley P, Noble A, Willett K. The biology of platelet-rich plasma and its application in trauma and orthopaedic surgery: a review of the literature. J Bone Joint Surg Br. 2009;91(8):987-996. 6. Andia I, Sanchez M, Maffulli N. Platelet rich plasma therapies for sports muscle injuries: any evidence behind clinical practice? Expert Opin Biol Ther. 2011;11(4):509-518. 7. 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(1):40-48. 8. Arnason A, Sigurdsson SB, Gudmundsson A, Holme I, Engebretsen L, Bahr R. Risk factors for injuries in football. Am J Sports Med. 2004;32(1 Suppl):5S-16S. 9. Askling C, Karlsson J, Thorstensson A. Hamstring injury occurrence in elite soccer players after preseason strength training with eccentric overload. Scand J Med Sci Sports. 2003;13(4):244-250. 10. Askling CM, Tengvar M, Saartok T, Thorstensson A. Acute first-time hamstring strains during slow-speed stretching: clinical, magnetic resonance imaging, and recovery characteristics. Am J Sports Med. 2007;35(10):1716-1724. 11. Bachrach E, Perez AL, Choi YH, et al. Muscle engraftment of myogenic progenitor cells following intraarterial transplantation. Muscle Nerve. 2006;34(1):44-52. 12. Bedair HS, Karthikeyan T, Quintero A, Li Y, Huard J. Angiotensin II receptor blockade administered after injury improves muscle regeneration and decreases fibrosis in normal skeletal muscle. Am J Sports Med. 2008;36(8):1548-1554. 13. Bennell K, Wajswelner H, Lew P, et al. Isokinetic strength testing does not predict hamstring injury in Australian rules footballers. Br J Sports Med. 1998;32(4):309-314. 14. Bintliff S, Walker BE. Radioautographic study of skeletal muscle regeneration. Am J Anat. 1960;106(3):233-245. 15. Birmingham P, Muller M, Wickiewicz T, Cavanaugh J, Rodeo S, Warren R. Functional outcome after repair of proximal hamstring avulsions. J Bone Joint Surg Am. 2011;93(19):1819-1826. 16. Blasier RB, Morawa LG. Complete rupture of the hamstring origin from a water skiing injury. Am J Sports Med. 1990;18(4):435-437. 17. Bradley PS, Portas MD. The relationship between preseason range of motion and muscle strain injury in elite soccer players. J Strength Cond Res. 2007;21(4):1155-1159. 18. Bresler M, Mar W, Toman J. Diagnostic imaging in the evaluation of leg pain in athletes. Clin Sports Med. 2012;31(2):217-245. 19. Brewer BJ. Mechanism of injury to the musculotendinous unit. Instr Course Lect. 1960;17:354-358. 20. Brockett CL, Morgan DL, Proske U. Human hamstring muscles adapt to eccentric exercise by changing optimum length. Med Sci Sports Exerc. 2001;33(5):783-790. 21. Brooks JH, Fuller CW, Kemp SP, Reddin DB. Incidence, risk, and prevention of hamstring muscle injuries in professional rugby union. Am J Sports Med. 2006;34(8):1297-1306. 22. Brubaker CE, James SL. Injuries to runners. J Sports Med. 1974;2(4):189-198. 23. Brucker PU, Imhoff AB. Functional assessment after acute and chronic complete ruptures of the proximal hamstring tendons. Knee Surg Sports Traumatol Arthrosc. 2005;13(5):411-418. 24. Burkett LN. Causative factors in hamstring strains. Med Sci Sports. 1970;2(1):39-42. 25. Burkett LN. Investigation into hamstring strains: the case of the hybrid muscle. J Sports Med. 1975;3(5):228-231. 26. Cacchio A, Borra F, Severini G, et al. Reliability and validity of three pain provocation tests used for the diagnosis of chronic proximal hamstring tendinopathy. Br J Sports Med. 2012;46(12):883-887. 27. Cacchio A, Rompe JD, Furia JP, Susi P, Santilli V, De Paulis F. Shockwave therapy for the treatment of chronic proximal hamstring
Vol. 41, No. 12, 2013
28.
29.
30.
31.
32. 33. 34. 35.
36.
37.
38.
39.
40. 41.
42.
43.
44. 45.
46.
47.
48.
49.
tendinopathy in professional athletes. Am J Sports Med. 2011;39(1):146-153. Cao B, Zheng B, Jankowski RJ, et al. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol. 2003;5(7):640-646. Chakravarthy J, Ramisetty N, Pimpalnerkar A, Mohtadi N. Surgical repair of complete proximal hamstring tendon ruptures in water skiers and bull riders: a report of four cases and review of the literature. Br J Sports Med. 2005;39(8):569-572. Chan O, Del Buono A, Best TM, Maffulli N. Acute muscle strain injuries: a proposed new classification system. Knee Surg Sports Traumatol Arthrosc. 2012;20(11):2356-2362. 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(16):35553562. Clanton TO, Coupe KJ. Hamstring strains in athletes: diagnosis and treatment. J Am Acad Orthop Surg. 1998;6(4):237-248. Clark WE. An experimental study of the regeneration of mammalian striped muscle. J Anat. 1946;80:24-36. Cohen S, Bradley J. Acute proximal hamstring rupture. J Am Acad Orthop Surg. 2007;15(6):350-355. Cohen SB, Rangavajjula A, Vyas D, Bradley JP. Functional results and outcomes after repair of proximal hamstring avulsions. Am J Sports Med. 2012;40(9):2092-2098. Cohen SB, Towers JD, Zoga A, et al. Hamstring injuries in professional football players: magnetic resonance imaging correlation with return to play. Sports Health. 2011;3(5):423-430. Connell DA, Schneider-Kolsky ME, Hoving JL, et al. Longitudinal study comparing sonographic and MRI assessments of acute and healing hamstring injuries. AJR Am J Roentgenol. 2004;183(4):975984. Cooper DE, Conway JE. Distal semitendinosus ruptures in elite-level athletes: low success rates of nonoperative treatment. Am J Sports Med. 2010;38(6):1174-1178. Cowin AJ, Holmes TM, Brosnan P, Ferguson MW. Expression of TGF-beta and its receptors in murine fetal and adult dermal wounds. Eur J Dermatol. 2001;11(5):424-431. Croisier JL. Factors associated with recurrent hamstring injuries. Sports Med. 2004;34(10):681-695. Croisier JL, Forthomme B, Namurois MH, Vanderthommen M, Crielaard JM. Hamstring muscle strain recurrence and strength performance disorders. Am J Sports Med. 2002;30(2):199-203. 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(8):14691475. Cross MJ, Vandersluis R, Wood D, Banff M. Surgical repair of chronic complete hamstring tendon rupture in the adult patient. Am J Sports Med. 1998;26(6):785-788. David A, Buchholz J, Muhr G. Tear of the biceps femoris tendon. Arch Orthop Trauma Surg. 1994;113(6):351-352. De Smet AA, Best TM. MR imaging of the distribution and location of acute hamstring injuries in athletes. AJR Am J Roentgenol. 2000;174(2):393-399. Ekstrand J, Gillquist J, Moller M, Oberg B, Liljedahl SO. Incidence of soccer injuries and their relation to training and team success. Am J Sports Med. 1983;11(2):63-67. Ekstrand J, Hagglund M, Walden M. Injury incidence and injury patterns in professional football: the UEFA injury study. Br J Sports Med. 2011;45(7):553-558. Elliott MC, Zarins B, Powell JW, Kenyon CD. Hamstring muscle strains in professional football players: a 10-year review. Am J Sports Med. 2011;39(4):843-850. Engebretsen AH, Myklebust G, Holme I, Engebretsen L, Bahr R. Intrinsic risk factors for hamstring injuries among male soccer
50.
51.
52. 53.
54.
55.
56.
57. 58.
59. 60.
61.
62.
63.
64. 65.
66.
67.
68.
69.
70. 71.
players: a prospective cohort study. Am J Sports Med. 2010;38(6): 1147-1153. Folsom GJ, Larson CM. Surgical treatment of acute versus chronic complete proximal hamstring ruptures: results of a new allograft technique for chronic reconstructions. Am J Sports Med. 2008; 36(1):104-109. Foreman TK, Addy T, Baker S, Burns J, Hill N, Madden T. Prospective studies into the causation of hamstring injuries in sport: a systematic review. Phys Ther Sport. 2006;7:101-109. Fortems Y, Victor J, Dauwe D, Fabry G. Isolated complete rupture of biceps femoris tendon. Injury. 1995;26(4):275-276. Frizziero A, Giannotti E, Oliva F, Masiero S, Maffulli N. Autologous conditioned serum for the treatment of osteoarthritis and other possible applications in musculoskeletal disorders [published online July 4, 2012]. Br Med Bull. doi:10.1093/bmb/lds016 Gabbe BJ, Bennell KL, Finch CF. Why are older Australian football players at greater risk of hamstring injury? J Sci Med Sport. 2006;9(4):327-333. Gabbe BJ, Bennell KL, Finch CF, Wajswelner H, Orchard JW. Predictors of hamstring injury at the elite level of Australian football. Scand J Med Sci Sports. 2006;16(1):7-13. Gabbe BJ, Finch CF, Bennell KL, Wajswelner H. Risk factors for hamstring injuries in community level Australian football. Br J Sports Med. 2005;39(2):106-110. Garrett WE Jr. Muscle strain injuries. Am J Sports Med. 1996;24(6 Suppl):S2-S8. Garrett WE Jr, Rich FR, Nikolaou PK, Vogler JB 3rd. Computed tomography of hamstring muscle strains. Med Sci Sports Exerc. 1989;21(5):506-514. Hamilton B, Knez W, Eirale C, Chalabi H. Platelet enriched plasma for acute muscle injury. Acta Orthop Belg. 2010;76(4):443-448. Harris JD, Griesser MJ, Best TM, Ellis TJ. Treatment of proximal hamstring ruptures: a systematic review. Int J Sports Med. 2011;32(7):490-495. Heiderscheit BC, Hoerth DM, Chumanov ES, Swanson SC, Thelen BJ, Thelen DG. Identifying the time of occurrence of a hamstring strain injury during treadmill running: a case study. Clin Biomech (Bristol, Avon). 2005;20(10):1072-1078. Heiser TM, Weber J, Sullivan G, Clare P, Jacobs RR. Prophylaxis and management of hamstring muscle injuries in intercollegiate football players. Am J Sports Med. 1984;12(5):368-370. Henderson G, Barnes CA, Portas MD. Factors associated with increased propensity for hamstring injury in English Premier League soccer players. J Sci Med Sport. 2010;13(4):397-402. Hoskins W, Pollard H. The management of hamstring injury, part 1: issues in diagnosis. Man Ther. 2005;10(2):96-107. Husmann I, Soulet L, Gautron J, Martelly I, Barritault D. Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev. 1996;7(3):249-258. Ishikawa K, Kai K, Mizuta H. Avulsion of the hamstring muscles from the ischial tuberosity: a report of two cases. Clin Orthop Relat Res. 1988;232:153-155. Jackson WM, Nesti LJ, Tuan RS. Potential therapeutic applications of muscle-derived mesenchymal stem and progenitor cells. Expert Opin Biol Ther. 2010;10(4):505-517. Jarvinen M. Healing of a crush injury in rat striated muscle, 3: a micro-angiographical study of the effect of early mobilization and immobilization on capillary ingrowth. Acta Pathol Microbiol Scand A. 1976;84(1):85-94. Kaminski TW, Wabbersen CV, Murphy RM. Concentric versus enhanced eccentric hamstring strength training: clinical implications. J Athl Train. 1998;33(3):216-221. Klingele KE, Sallay PI. Surgical repair of complete proximal hamstring tendon rupture. Am J Sports Med. 2002;30(5):742-747. Knapik JJ, Jones BH, Bauman CL, Harris JM. Strength, flexibility and athletic injuries. Sports Med. 1992;14(5):277-288.
2946 Ahmad et al
72. Kusma M, Seil R, Kohn D. Isolated avulsion of the biceps femoris insertion-injury patterns and treatment options: a case report and literature review. Arch Orthop Trauma Surg. 2007;127(9):777-780. 73. Kuszewski M, Gnat R, Saulicz E. Stability training of the lumbo-pelvohip complex influence stiffness of the hamstrings: a preliminary study. Scand J Med Sci Sports. 2009;19(2):260-266. 74. Lephart SM, Abt JP, Ferris CM, et al. Neuromuscular and biomechanical characteristic changes in high school athletes: a plyometric versus basic resistance program. Br J Sports Med. 2005;39(12):932938. 75. Levine WN, Bergfeld JA, Tessendorf W, Moorman CT 3rd. Intramuscular corticosteroid injection for hamstring injuries: a 13-year experience in the National Football League. Am J Sports Med. 2000;28(3):297-300. 76. Li Y, Foster W, Deasy BM, et al. Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am J Pathol. 2004;164(3):1007-1019. 77. Liemohn W. Factors related to hamstring strains. J Sports Med Phys Fitness. 1978;18(1):71-76. 78. Lim BO, Lee YS, Kim JG, An KO, Yoo J, Kwon YH. Effects of sports injury prevention training on the biomechanical risk factors of anterior cruciate ligament injury in high school female basketball players. Am J Sports Med. 2009;37(9):1728-1734. 79. Longo UG, Garau G, Denaro V, Maffulli N. Surgical management of tendinopathy of biceps femoris tendon in athletes. Disabil Rehabil. 2008;30(20-22):1602-1607. 80. Longo UG, Loppini M, Berton A, Marinozzi A, Maffulli N, Denaro V. The FIFA 111 program is effective in preventing injuries in elite male basketball players: a cluster randomized controlled trial. Am J Sports Med. 2012;40(5):996-1005. 81. Longo UG, Loppini M, Berton A, Spiezia F, Maffulli N, Denaro V. Tissue engineered strategies for skeletal muscle injury. Stem Cells International. 2012;2012:13. 82. Lu L, Saulis AS, Liu WR, et al. The temporal effects of anti-TGFbeta1, 2, and 3 monoclonal antibody on wound healing and hypertrophic scar formation. J Am Coll Surg. 2005;201(3):391-397. 83. Maffulli N, Longo UG, Gougoulias N, Caine D, Denaro V. Sport injuries: a review of outcomes. Br Med Bull. 2011;97:47-80. 84. Maffulli N, Longo UG, Gougoulias N, Loppini M, Denaro V. Long-term health outcomes of youth sports injuries. Br J Sports Med. 2010;44(1):21-25. 85. Maffulli N, Longo UG, Spiezia F, Denaro V. Aetiology and prevention of injuries in elite young athletes. Med Sport Sci. 2011;56:187-200. 86. Maffulli N, Longo UG, Spiezia F, Denaro V. Sports injuries in young athletes: long-term outcome and prevention strategies. Phys Sportsmed. 2010;38(2):29-34. 87. Mair SD, Seaber AV, Glisson RR, Garrett WE Jr. The role of fatigue in susceptibility to acute muscle strain injury. Am J Sports Med. 1996;24(2):137-143. 88. Mann G, Shabat S, Friedman A, et al. Hamstring injuries. Orthopedics. 2007;30(7):536-540, quiz 541-532. 89. Mariani C, Caldera FE, Kim W. Ultrasound versus magnetic resonance imaging in the diagnosis of an acute hamstring tear. PM R. 2012;4(2):154-155. 90. Mason DL, Dickens V, Vail A. Rehabilitation for hamstring injuries. Cochrane Database Syst Rev. 2007;(1):CD004575. 91. McGoldrick F, Colville J. Spontaneous rupture of the biceps femoris. Arch Orthop Trauma Surg. 1990;109(4):234. 92. McGregor C, Ghosh S, Young DA, Maffulli N. Traumatic and overuse injuries of the ischial origin of the hamstrings. Disabil Rehabil. 2008;30(20-22):1597-1601. 93. Mejia HA, Bradley JP. The effects of platelet-rich plasma on muscle: basic science and clinical application. Oper Tech Sports Med. 2011;19:149-153. 94. Mendiguchia J, Alentorn-Geli E, Brughelli M. Hamstring strain injuries: are we heading in the right direction? Br J Sports Med. 2012;46(2):81-85.
95. Mendiguchia J, Brughelli M. A return-to-sport algorithm for acute hamstring injuries. Phys Ther Sport. 2011;12(1):2-14. 96. Miller SL, Gill J, Webb GR. The proximal origin of the hamstrings and surrounding anatomy encountered during repair: a cadaveric study. J Bone Joint Surg Am. 2007;89(1):44-48. 97. Mjolsnes R, Arnason A, Osthagen 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;14(5):311-317. 98. Nichols AW. Complications associated with the use of corticosteroids in the treatment of athletic injuries. Clin J Sport Med. 2005;15(5):370-375. 99. Orchard J, Marsden J, Lord S, Garlick D. Preseason hamstring muscle weakness associated with hamstring muscle injury in Australian footballers. Am J Sports Med. 1997;25(1):81-85. 100. Orchard J, Steet E, Walker C, Ibrahim A, Rigney L, Houang M. Hamstring muscle strain injury caused by isokinetic testing. Clin J Sport Med. 2001;11(4):274-276. 101. Orchard JW. Intrinsic and extrinsic risk factors for muscle strains in Australian football. Am J Sports Med. 2001;29(3):300-303. 102. Puranen J, Orava S. The hamstring syndrome: a new diagnosis of gluteal sciatic pain. Am J Sports Med. 1988;16(5):517-521. 103. Rossi CA, Pozzobon M, De Coppi P. Advances in musculoskeletal tissue engineering: moving towards therapy. Organogenesis. 2010; 6(3):167-172. 104. Safran MR, Seaber AV, Garrett WE Jr. Warm-up and muscular injury prevention: an update. Sports Med. 1989;8(4):239-249. 105. Sallay PI, Ballard G, Hamersly S, Schrader M. Subjective and functional outcomes following surgical repair of complete ruptures of the proximal hamstring complex. Orthopedics. 2008;31(11):1092. 106. Sallay PI, Friedman RL, Coogan PG, Garrett WE. Hamstring muscle injuries among water skiers: functional outcome and prevention. Am J Sports Med. 1996;24(2):130-136. 107. Sarimo J, Lempainen L, Mattila K, Orava S. Complete proximal hamstring avulsions: a series of 41 patients with operative treatment. Am J Sports Med. 2008;36(6):1110-1115. 108. Schache AG, Wrigley TV, Baker R, Pandy MG. Biomechanical response to hamstring muscle strain injury. Gait Posture. 2009; 29(2):332-338. 109. Schilders E, Bismil Q, Sidhom S, Robinson P, Barwick T, Talbot C. Partial rupture of the distal semitendinosus tendon treated by tenotomy: a previously undescribed entity. Knee. 2006;13(1):45-47. 110. Sekhon JS, Anderson K. Rupture of the distal semitendinosus tendon: a report of two cases in professional athletes. J Knee Surg. 2007;20(2):147-150. 111. Shelly MJ, Hodnett PA, MacMahon PJ, Moynagh MR, Kavanagh EC, Eustace SJ. MR imaging of muscle injury. Magn Reson Imaging Clin N Am. 2009;17(4):757-773, vii. 112. Sherry MA, Best TM. A comparison of 2 rehabilitation programs in the treatment of acute hamstring strains. J Orthop Sports Phys Ther. 2004;34(3):116-125. 113. Slavotinek JP, Verrall GM, Fon GT. Hamstring injury in athletes: using MR imaging measurements to compare extent of muscle injury with amount of time lost from competition. AJR Am J Roentgenol. 2002;179(6):1621-1628. 114. Soligard T, Myklebust G, Steffen K, et al. Comprehensive warm-up programme to prevent injuries in young female footballers: cluster randomised controlled trial. BMJ. 2008;337:a2469. 115. Standaert CJ. Shockwave therapy for chronic proximal hamstring tendinopathy. Clin J Sport Med. 2012;22(2):170-171. 116. Stauber WT. Repair models and specific tissue responses in muscle injury. In: Leadbetter WB, Buckwalter JA, Gordon SL, eds. SportsInduced Inflammation: Clinical and Basic Science Concepts. Park Ridge, Illinois: American Academy of Orthopaedic Surgeons; 1990:205-213. 117. Steffen K, Myklebust G, Olsen OE, Holme I, Bahr R. Preventing injuries in female youth football: a cluster-randomized controlled trial. Scand J Med Sci Sports. 2008;18(5):605-614.
Vol. 41, No. 12, 2013
118. Sugiura Y, Saito T, Sakuraba K, Sakuma K, Suzuki E. Strength deficits identified with concentric action of the hip extensors and eccentric action of the hamstrings predispose to hamstring injury in elite sprinters. J Orthop Sports Phys Ther. 2008;38(8):457-464. 119. Tegnander A, Olsen OE, Moholdt TT, Engebretsen L, Bahr R. Injuries in Norwegian female elite soccer: a prospective one-season cohort study. Knee Surg Sports Traumatol Arthrosc. 2008; 16(2):194-198. 120. Terry GC, LaPrade RF. The biceps femoris muscle complex at the knee: its anatomy and injury patterns associated with acute anterolateral-anteromedial rotatory instability. Am J Sports Med. 1996;24(1):2-8. 121. Torrente Y, Tremblay JP, Pisati F, et al. Intraarterial injection of muscle-derived CD34(1)Sca-1(1) stem cells restores dystrophin in mdx mice. J Cell Biol. 2001;152(2):335-348. 122. Verrall GM, Slavotinek JP, Barnes PG, Fon GT. Diagnostic and prognostic value of clinical findings in 83 athletes with posterior thigh injury: comparison of clinical findings with magnetic resonance imaging documentation of hamstring muscle strain. Am J Sports Med. 2003;31(6):969-973. 123. Verrall GM, Slavotinek JP, Barnes PG, Fon GT, Spriggins AJ. Clinical risk factors for hamstring muscle strain injury: a prospective study with correlation of injury by magnetic resonance imaging. Br J Sports Med. 2001;35(6):435-439, discussion 440. 124. Warren LF, Marshall JL. The supporting structures and layers on the medial side of the knee: an anatomical analysis. J Bone Joint Surg Am. 1979;61(1):56-62.
125. Wetzel RJ, Patel RM, Terry MA. Platelet-rich plasma as an effective treatment for proximal hamstring injuries. Orthopedics. 2013;36(1): e64-e70. 126. Witvrouw E, Danneels L, Asselman P, DHave T, Cambier D. Muscle flexibility as a risk factor for developing muscle injuries in male professional soccer players: a prospective study. Am J Sports Med. 2003;31(1):41-46. 127. Wood DG, Packham I, Trikha SP, Linklater J. Avulsion of the proximal hamstring origin. J Bone Joint Surg Am. 2008;90(11):2365-2374. 128. Woods C, Hawkins RD, Maltby S, et al. The Football Association Medical Research Programme. An audit of injuries in professional football: analysis of hamstring injuries. Br J Sports Med. 2004;38(1):36-41. 129. Worrell TW. Factors associated with hamstring injuries: an approach to treatment and preventative measures. Sports Med. 1994;17(5):338-345. 130. Worrell TW, Perrin DH, Gansneder BM, Gieck JH. Comparison of isokinetic strength and flexibility measures between hamstring injured and noninjured athletes. J Orthop Sports Phys Ther. 1991;13(3):118-125. 131. Yeung SS, Suen AM, Yeung EW. A prospective cohort study of hamstring injuries in competitive sprinters: preseason muscle imbalance as a possible risk factor. Br J Sports Med. 2009; 43(8):589-594. 132. Zarins B, Ciullo JV. Acute muscle and tendon injuries in athletes. Clin Sports Med. 1983;2(1):167-182. 133. Zissen MH, Wallace G, Stevens KJ, Fredericson M, Beaulieu CF. High hamstring tendinopathy: MRI and ultrasound imaging and therapeutic efficacy of percutaneous corticosteroid injection. AJR Am J Roentgenol. 2010;195(4):993-998.
For reprints and permission queries, please visit SAGEs Web site at http://www.sagepub.com/journalsPermissions.nav

Evaluation and Management of Hamstring Injuries

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Evaluation and Management of Hamstring Injuries

Uploaded by

Copyright:

Available Formats

The American Journal of Sports Medicine

http://ajs.sagepub.com/ Evaluation and Management of Hamstring Injuries

American Orthopaedic Society for Sports Medicine

Downloaded from ajs.sagepub.com at Tel Aviv University on December 16, 2013

Clinical Sports Medicine Update