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http://ajs.sagepub.com/ Medicine The American Journal of Sports http://ajs.sagepub.com/content/41/12/2933 The online version of this article can be found at: DOI: 10.1177/0363546513487063 2013 41: 2933 originally published online May 23, 2013 Am J Sports Med Bradley Christopher S. Ahmad, Lauren H. Redler, Michael G. Ciccotti, Nicola Maffulli, Umile Giuseppe Longo and James Evaluation and Management of Hamstring Injuries Published by: http://www.sagepublications.com On behalf of: American Orthopaedic Society for Sports Medicine can be found at: The American Journal of Sports Medicine Additional services and information for http://ajs.sagepub.com/cgi/alerts Email Alerts: http://ajs.sagepub.com/subscriptions Subscriptions: http://www.sagepub.com/journalsReprints.nav Reprints: http://www.sagepub.com/journalsPermissions.nav Permissions: What is This? - May 23, 2013 OnlineFirst Version of Record - Nov 27, 2013 Version of Record >> at Tel Aviv University on December 16, 2013 ajs.sagepub.com Downloaded from at Tel Aviv University on December 16, 2013 ajs.sagepub.com Downloaded from

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Evaluation and Management of Hamstring Injuries

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Page 1: Evaluation and Management of Hamstring Injuries

http://ajs.sagepub.com/Medicine

The American Journal of Sports

http://ajs.sagepub.com/content/41/12/2933The online version of this article can be found at:

 DOI: 10.1177/0363546513487063

2013 41: 2933 originally published online May 23, 2013Am J Sports MedBradley

Christopher S. Ahmad, Lauren H. Redler, Michael G. Ciccotti, Nicola Maffulli, Umile Giuseppe Longo and JamesEvaluation and Management of Hamstring Injuries

  

Published by:

http://www.sagepublications.com

On behalf of: 

  American Orthopaedic Society for Sports Medicine

can be found at:The American Journal of Sports MedicineAdditional services and information for    

  http://ajs.sagepub.com/cgi/alertsEmail Alerts:

 

http://ajs.sagepub.com/subscriptionsSubscriptions:  

http://www.sagepub.com/journalsReprints.navReprints:  

http://www.sagepub.com/journalsPermissions.navPermissions:  

What is This? 

- May 23, 2013OnlineFirst Version of Record  

- Nov 27, 2013Version of Record >>

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

Page 2: Evaluation and Management of Hamstring Injuries

Evaluation and Managementof 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,{ MDInvestigation performed at the Center for Shoulder, Elbow, and Sports Medicine, Departmentof 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. Theseinjuries lead to prolonged impairment and have a reinjury risk of 12% to 31%. They range from mild muscle damage without lossof structural integrity to complete muscle tearing with fiber disruption. Novel MRI scores are increasingly being used and allowa more precise prediction of return to sport. In this article, the authors review the history, mechanisms of injury, and classificationsystems for hamstring injuries as well as present the latest evidence related to the management of hamstring injuries, includingintramuscular and both proximal and distal insertional injuries. Indications for surgical treatment of certain proximal and distalavulsions, biological augmentation to the nonoperative treatment of midsubstance injuries, and advances in risk reduction andinjury prevention are discussed.

Keywords: hamstring; biceps femoris; semimembranosus; semitendinosus; platelet-rich plasma; cell therapy; hamstring injuryprevention; proximal hamstring repair; distal hamstring resection

Hamstring injuries are among the most common lowerextremity injuries in athletes,3,32,34,57,132 accounting forup to 29% of all injuries in various sports21,40,57,99,100,128;in addition, they may produce prolonged impairment andan immense reinjury risk of 12% to 31%.40,48,128 Theseinjuries are most common in sports requiring rapid acceler-ation such as running, hurdling, jumping, and kickingsports. Hamstring strains account for 50% of muscle inju-ries in sprinters and are the most common injury in hur-dling.22 Most hamstring strains in the United StatesNational Football League (NFL) are sustained during non-contact activities, with sprinting as the primary activity.48

‘‘Speed positions’’ (receivers, defensive backs, and runningbacks) have significantly higher rates of hamstring musclestrains compared with ‘‘strength positions’’ (offensive anddefensive linemen). Sports with ballistic movements such

as skiing, dancing, skating, and weight lifting are associ-ated with hamstring injuries, particularly the proximalavulsion type.3,34

The injuries range from mild muscle damage withoutloss of structural integrity to complete muscle tearingwith fiber disruption. Reductions in the incidence, severity,and reinjury risk of hamstring injuries have obvious poten-tial to reduce medical costs and time lost from sport.Advances in diagnosis, classification, newer surgical andbiological treatments, as well as prevention strategiesmay 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 semi-membranosus. All 3 muscles, except for the short head ofthe biceps femoris, originate from the ischial tuberosityas a common tendon. They then separate 5 to 10 cm distalto the ischium, with the semimembranosus first to becomedistinct.58 The muscle fibers of the biceps femoris are visi-ble 6 cm distal to the tuberosity, and the proximal myoten-dinous junction encompasses approximately 60% of thetotal length of the muscle.58 The semimembranosus musclefibers appear within the proximal 30% of this muscle, andthe semitendinosus muscle fibers insert directly to theischial tuberosity at the proximal musculotendinous junc-tion.58 The short head of the biceps femoris originatesjust medial to the linea aspera in the posterior distalfemur. The long head of the biceps femoris attaches tothe fibular head and the lateral tibia.120 The short head

M

yAddress 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: [email protected]).

*Center for Shoulder, Elbow, and Sports Medicine, Department ofOrthopaedic Surgery, Columbia University, New York, New York.

zCenter for Sports Medicine, Rothman Institute, Department of Ortho-paedic 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 Uni-versity, Rome, Italy.

{Center for Sports Medicine, University of Pittsburgh Medical Center,Pittsburgh, Pennsylvania.

The authors declared that they have no conflicts of interest in theauthorship and publication of this contribution.

The American Journal of Sports Medicine, Vol. 41, No. 12DOI: 10.1177/0363546513487063� 2013 The Author(s)

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of the biceps femoris attaches into the tendon of the longhead of the biceps femoris as well as fascial and tendinousinsertions to the posterolateral capsule, the iliotibial tract,the fibular head, and the proximal lateral tibia.120 Thesemimembranosus has multiple insertions at the postero-medial corner of the knee.124 The semitendinosus joinsthe sartorius and gracilis tendons to form the pes anseri-nus on the medial aspect of the proximal tibia, overlyingthe medial collateral ligament. The distal musculotendi-nous complex covers approximately 66% of the length ofthe biceps femoris and slightly more than 50% of the lengthof the semimembranosus and semitendinosus muscles.124

The semimembranosus, semitendinosus, and long headof the biceps femoris are innervated by the tibial portion ofthe sciatic nerve, and the short head of the biceps is inner-vated by the peroneal portion of the sciatic nerve. Thesemimembranosus adds stability to the knee and functionsto flex and medially rotate the leg at the knee as well asextending, adducting, and medially rotating the thigh atthe hip.2,32,88 The semitendinosus is a flexor and internalrotator of the tibia at the knee and also provides valgusstability to the knee.2,32,88 The short head of the bicepsfunctions to flex the knee with the thigh extended; thelong head gives posterior stability to the pelvis and extendsthe femur at the hip.2,32,88

Mechanism of Injury

The hamstring muscle group spans both the hip and kneejoints, producing potential for rapid and extreme musclelengthening. Injury occurs most commonly during eccen-tric muscle contraction.57,132 During the last 25% of theswing phase, the hamstrings assist in proximal hip exten-sion while decelerating knee extension distally. The ham-strings remain active during the first half of the stancephase to produce hip extension and resist knee extensionthrough a concentric contraction.2 Sprint mechanicsresearch suggests that strain injury risk is greatest nearthe end of the swing phase, when the hamstrings reachmaximal length and undergo eccentric contraction justbefore heel strike.61,108 The mechanism of proximal avul-sions is through an eccentric contraction with the hipflexed and the knee extended and occurs with higherenergy ballistic activities.#

Pathological Changes

The myotendinous junction experiences the highest eccen-tric loads and is the most common location ofinjury.32,34,36,38,89 Muscle belly injuries are less commonbut can occur with direct trauma or contusion.3,32 Com-plete ruptures are rare and tend to occur with pre-existingtendinopathy. In the simplest injury, only the myofibrilsare damaged, resulting in leakage of the cytoplasmicenzyme creatine kinase. With greater injury severity, theextracellular matrix and fascia become damaged, followedby release of muscle enzymes, collagen and proteoglycan

degradation, and inflammation. Blood vessel damageresults in bleeding and clotting. A local ischemic environ-ment can result, causing further muscle damage andedema. The healing process involves muscle regenerationand fibrosis. A properly aligned extracellular matrix isrequired to maintain optimal myofibril orientation. Withan intact or repaired basal lamina acting as a scaffold,myofibrils can regenerate. Early range of motion afterinjury can minimize disorganized scar formation andreinjury.116

Risk Factors for Injury

A variety of risk factors have been proposed for hamstringinjuries, including inadequate warm-up, strength imbal-ance, lower extremity flexibility,17,63,126 core stabil-ity,38,64,90,112 muscle weakness,41,42,99 fatigue,87,128,132

dehydration, and a history of injury.8,13,49,55,101 Strengthimbalance refers to either a difference in hamstringstrength between lower extremities or an altered ratio ofhamstring-to-quadriceps strength in the same extrem-ity.32,77,129 Thresholds of side-to-side hamstring deficits of.10% to 15% or a hamstring-to-quadriceps strength ratioof \0.6 increase the injury risk.24,32,71,77 These ratios, how-ever, most likely vary with sex, sport, and position played.**

Muscle weakness40,42,118,131 and, more recently, poorcore stability have been associated with hamstring inju-ries.31,64,90,112 Lumbopelvic position, which is in part con-trolled by abdominal muscle activity, may influencehamstring muscle length and stiffness.31,73 Fatigue isa risk factor, and more hamstring injuries occur towardthe end of an athletic competition.47,128 Animal studieshave demonstrated that eccentric loads of fatigued musclesresult in significantly more damage than isometric or con-centric loads.46,104 Similarly, increasing muscle tempera-ture may increase the ability of the muscle tendon unitto absorb force.46,104

Flexibility remains controversial as a risk factor. Pro-spective studies8,13,49,55,56,99,131 demonstrate no relation-ship between flexibility of the knee flexors and hamstringinjury, but other studies have shown an associationbetween flexibility values obtained in preseason trainingand injuries suffered during the season.17,63,126,129,130 Inaddition, an association between reduced hip flexor flexi-bility and the risk of hamstring injuries has beenreported.54

Seasonal timing of hamstring strains has been demon-strated in the NFL, with the preseason identified as themost vulnerable period.48 Factors implicated in this trendare the relative deconditioning and muscle weakness thatoccur in the off-season.

Perhaps the most significant risk factor is a previoushamstring injury, which increases the risk of reinjury by2 to 6 times.7,13,49,55,101 A previous hamstring injury maylead to the formation of weakened scar tissue at the injurysite, thereby lowering the threshold to a recurrentinjury.3,21,49,51,56,123

#References 22, 32, 34, 66, 88, 106, 107, 127, 132. **References 2, 19, 24, 25, 32, 40, 62, 71, 88, 104, 132.

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Clinical Presentation

History. Most athletes experience acute, sudden sharppain in the posterior thigh, often with an audible or palpa-ble pop,32,129 during an activity requiring a combination ofsudden hip flexion and knee extension as in running, jump-ing, and kicking sports.3,32,129 A smaller number note aninsidious 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, par-ticularly with recurrent mild episodes of injury. Proximalavulsion injuries may cause discomfort with sitting. Ath-letes often describe difficulty in walking smoothly.

Physical Examination. Inspection begins with anassessment of gait with a ‘‘stiff-legged’’ gait pattern oftennoted as the athlete attempts to avoid simultaneous hipflexion and knee extension.3,34 Most often, minimal ecchy-mosis is observed; however, broad ecchymosis along theposterior thigh may be encountered and may indicatea high-grade myotendinous injury or a proximal avulsioninjury (Figure 1). In cases of a muscle belly rupture,a defect may be palpable.32 With either proximal or,

more commonly, distal avulsion, a thickened area of subcu-taneous tissue may be identified adjacent to theinjury.34,36,38

Palpation of the injured posterior thigh from the ischialtuberosity to the posterior aspect of the knee localizes theinjury by eliciting either tenderness or appreciatinga defect. Precise location is often difficult, given the deeplocation of the muscles, especially proximally. The rangeof motion of both lower extremities should be assessed. Acareful comparison of side-to-side symmetry of the hipsand knees will help to estimate the severity of the injury.The popliteal angle is determined by flexing the hip to90� with the knee flexed to 90� and then slowly extendingthe knee passively. The knee flexion angle at which poste-rior thigh pain and guarding occur is compared with thatin the contralateral, uninjured leg. An increased angle onthe affected side suggests a hamstring injury.32

Hamstring strength should then be assessed with thepatient in the prone position and the knee flexed to 90�.Resisted active knee flexion may help to more preciselydetermine the location and severity of the injury. Activeknee flexion while the examiner extends the knee to 30�reproduces the common eccentric load mechanism andalso aids in diagnosis. These maneuvers should be com-pared with the uninjured limb.

Several special provocation tests have more recentlybeen proposed to evaluate hamstring injuries, particularlytendinopathy and milder strains.26 The Puranen-Oravatest (Figure 2) is performed by an active stretch of thehamstrings with the patient standing. The hip is flexedto 90�; the knee is then fully actively extended, and theheel is held on a support. The bent-knee stretch test (Fig-ure 3) is performed with the patient supine. The hip andknee of the symptomatic extremity are maximally flexed,and the knee is then slowly passively extended by theexaminer. The modified bent-knee stretch test (Figure 4)is also performed with the patient supine and the symp-tomatic leg fully extended. The examiner maximally flexesthe hip and knee and then rapidly extends the knee. With

Figure 1. Clinical appearance of diffuse posterior thighecchymosis with a proximal myotendinous hamstring injury.

Figure 2. The Puranen-Orava test for hamstring tendinop-athy and strain.

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respect to all 3 tests, hamstring tendinopathy or strain isindicated by increasing posterior thigh pain with extensionof the knee. All 3 tests have been shown to have moderate to

high validity and reliability in identifying hamstring ten-dinopathy and strains.26 Finally, it is important to performa thorough neurovascular examination; peroneal nerve

Figure 3. Bent-knee stretch test for hamstring tendinopathy and strain.

Figure 4. Modified bent-knee stretch test for hamstring tendinopathy and strain.

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injury, while usually a neurapraxia and self-limiting, canresult in subtle foot drop or eversion weakness.

The differential diagnosis for hamstring injuriesincludes a variety of lesions occurring proximally at thehip and pelvis, along the posterior thigh, or distally atthe knee. Proximal injuries include ischial tuberosity apo-physitis, painful unfused apophysis, piriformis syndrome,gluteus medius insertional tendinopathy, posterior tro-chanteric bursitis, sacroiliitis, pelvic stress fracture, andlumbar radiculopathy. Posterior thigh injuries include ilio-tibial band syndrome, lumbar radiculopathy, and sciatica.Distal injuries include knee capsular strain, knee collat-eral ligament sprain, knee meniscal injury, lumbar radi-culopathy, gastrocnemius strain, popliteal cyst formationor rupture, and pes anserine bursitis.

Imaging. Plain radiographic findings of the pelvis, hip,femur, and knee are most often negative in athletes withhamstring injuries,3,32,34 unless an avulsion fracture hasoccurred from the ischial tuberosity (Figure 5). Dynamicultrasonography provides high-resolution imaging with

the advantages of direct correlation with physical exami-nation and perhaps access to more immediate imagingfrom portable ultrasound machines. Typically, hamstringmuscles and tendons are imaged using a linear probe inboth the longitudinal and transverse planes with

Figure 5. Plain radiograph of the pelvis, demonstrating anavulsion injury from the ischial tuberosity.

Figure 6. Longitudinal ultrasound image of a proximal myo-tendinous hamstring injury. A high-grade tear is identified bythe large white arrow, intact muscle is indicated by arrow-heads, and the tendon origin (*) is seen at the ischial tuber-osity (Tub).

Figure 7. Proximal hamstring (semimembranosus) avulsioninjury with retraction on coronal T2-weighted magnetic reso-nance imaging.

Figure 8. Cross-sectional muscle involvement on axial T2-weighted magnetic resonance imaging.

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frequencies in the 7.5- to 13-MHz range.3,89 Higher fre-quencies provide better resolution, while lower frequenciesprovide better penetration. Ultrasound demonstrates fluidcollections around and along the injured muscle anddepicts areas of echogenicity, representing edema and/orhemorrhage (Figure 6). Ultrasonography is extremelyaccurate in the acute phase to determine the location andextent of a hamstring injury.3,89 Magnetic resonance imag-ing (MRI), however, is the most commonly used imagingstudy to evaluate hamstring injuries. Standard axial, coro-nal, and sagittal T1- and T2-weighted images are obtainedon a 1.5-T or higher unit. For proximal hamstring injuries,images are obtained through both ischial tuberosities andproximal thighs; for distal injuries, images are obtainedfrom the midthigh through the knee. Higher resolutionimages are then obtained through the injured thigh.Also, MRI precisely defines the injury location, degree ofdamage, number of involved tendons, extent of retraction,and chronicityyy (Figures 7 and 8). With respect to loca-tion, MRI can precisely identify the injury site from the ori-gin, proximal myotendinous junction, muscle belly, distaljunction, or insertion (Figure 9). Moreover, MRI can deter-mine the degree of soft tissue damage by defining (1)dimensions of abnormal intramuscular and extramuscularT2 hyperintensity, (2) percentage of abnormal cross-sectional muscle area, (3) percentage of abnormal musclevolume, and (4) length of extramuscular T2 signaling113;

MRI can also determine the chronicity of injury as indi-cated by fibrosis.38 Further, MRI better defines a boneinjury seen with proximal or distal avulsions as well asmore delayed soft tissue changes seen with more chronicinjuries and can assess progressive healing.18,37,89

CLASSIFICATION

Hamstring injuries have traditionally been classified withrespect to their clinical presentation: (1) grade 1 (mild) ascharacterized by overstretching but minimal loss of thestructural 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 gener-ally accepted MRI grading system for muscle injuryincludes (1) grade 1 as defined by a T2 hyperintense signalabout a tendon or muscle without fiber disruption, (2)grade 2 as represented by a T2 hyperintense signal aroundand within a tendon/muscle with fiber disruption less thanhalf the tendon/muscle width, and (3) grade 3 as defined bytendon/muscle disruption less than half its width.111 Alter-natively, hamstring injuries can be classified based on theanatomic site, pattern, and severity of the injury in theacute stage, as assessed by MRI or ultrasound.30

Important to the management of hamstring strains isthe early determination of time required to return to fullcompetition. Neither the traditional clinical nor the gen-eral MRI classifications have been precisely correlated

Figure 9. (A) Proximal myotendinous hamstring injury on coronal T2-weighted magnetic resonance imaging (MRI). (B) Musclebelly injury on axial T2-weighted MRI. (C) Distal avulsion hamstring injury on coronal T2-weighted MRI.

TABLE 1Magnetic Resonance Imaging Scoring System for Hamstring Injuries

Points Age, yNo. of Muscles

Involved LocationInsertion

InvolvementCross-sectional

Injury, %Retraction,

cmLong-Axis T2Length, cm

0 No 0 None 01 �25 1 Proximal 25 \2 1-52 26-31 2 Middle Yes 50 �2 6-103 �32 3 Distal �75 .10

yyReferences 3, 18, 32, 34, 36, 45, 89, 111, 113.

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with time to return to play after a hamstring injury. Sev-eral authors have attempted to assess the predictive valueof MRI for return to play in athletes with these inju-ries.10,18,36,113,122 Verrall et al122 evaluated 83 elite Austra-lian rules football players with clinically diagnosedhamstring strains and observed that those athletes whohad MRI features of a hamstring injury averaged 27 daysmissed from competition and those with no changes onMRI missed an average of 16 days. Askling et al10 prospec-tively evaluated 18 elite sprinters with clinically diagnosedhamstring strains and serial MRI evaluations at 10, 21,and 42 days after injury. Proximal injuries demonstrateda prolonged time to return to play. Verall et al123 usedMRI to assess the volume and percentage of muscle injuryand found it was predictive of time lost from competition.Slavotinek et al113 also noted that the percentage of abnor-mal muscle area and the volume of injury correlated mostprecisely with time to return to sport, but no classificationwas proposed.

Cohen et al36 have provided the most detailed MRI clas-sification system that correlates the extent of hamstringinjury with time to return to play. These authors evaluated38 NFL players with acute hamstring strains. Their MRIscans were evaluated with the traditional radiologicalmuscle injury grading system as well as a new MRI scoringsystem. This scoring system (Table 1) was based on (1)player age, (2) number of muscles involved, (3) location ofinjury, (4) presence of insertional damage, (5) percentageof cross-sectional muscle involvement, (6) length of muscleretraction, (7) long-axis T2 sagittal plane signal abnormal-ities, and (8) presence of chronic changes. All scores werethen correlated with time missed from competition. Theseauthors noted that rapid return to play (\1 week) corre-lated with isolated injury of the long head of the bicepsfemoris, \50% cross-sectional involvement, and minimalperimuscular edema (grade 1 traditional radiologicalstrain) and an MRI score of \10. Prolonged recovery(.2-3 weeks) correlated with multiple-muscle injury, inju-ries distal to the myotendinous junction, short head of thebiceps injury, .75% cross-sectional involvement, presenceof retraction, circumferential edema (grade 3 traditionalradiological strain), and an MRI score of .15. Theseauthors suggested that this novel MRI score is highly pre-dictive of time missed from competition. Additional futuresystematic studies for different sports will be important forthe validation of this MRI score in predicting return to playfor other athletes.

Treatment: Noninsertional Injuries

Initial nonoperative treatment includes activity modifica-tion, ice, compression, stretching, early physical therapy,and nonsteroidal anti-inflammatory drugs (NSAIDs) withsport-specific activity progression carried out with atten-tion to the athlete’s symptoms. Other modalities includemassage, ultrasound, and electrical stimulation. A recentrandomized controlled trial showed shockwave therapy tobe safe, effective, and superior to traditional modalitiesin professional athletes with proximal hamstring

tendinopathies.27 Intramuscular corticosteroid injectionhas also been advocated as an early treatment to preventprolonged disability.65,75 Potential risks include infection,subsequent tendon rupture, increased likelihood of a recur-rent hamstring injury, postinjection pain flare, subcutane-ous fat atrophy, and skin hypopigmentation.98 Theproposed beneficial mechanism is mediation of the painfulinflammatory response triggered by the acute musclestrain. In the NFL, in players with severe discrete injurieswithin the substance of the muscle, intramuscular cortico-steroid injection decreased time to return to full play with-out a risk of further injuries or complications.75

Traditional management has been disappointing, withunpredictable time lost, high reinjury rates, and poor res-toration of preinjury status. New biological therapies aretherefore being investigated, including platelet-richplasma (PRP) treatment, cell therapy, tissue engineering,and administration of growth factors.81 Bioactive mole-cules include transforming growth factor–b (TGF-b), fibro-blast growth factor (FGF), epidermal growth factor (EGF),platelet-derived growth factor (PDGF), and vascular endo-thelial growth factor (VEGF). These play a crucial role inthe repair process of injured skeletal muscle, includinghamstring strains, namely by stimulating myogenesis65

and neoangiogenesis.68 Thus, they represent a potentialtherapeutic option in improving the healing process.

Platelet-Rich Plasma. Platelet-rich plasma is a concen-trated source of autologous platelets and the growth fac-tors that their a granules naturally contain. Given thesebioactive molecules, PRP has the potential to improve thehealing process, and thus, its use has been proposed forthe management of many musculoskeletal injuries, includ-ing hamstring strains.59,125 Although its efficacy has notbeen proven, PRP has been widely described in the ortho-paedic literature because of its ease of acquisition andsafety.6,53 Mejia and Bradley93 reported on their experi-ence with autologous conditioned plasma injections within24 to 48 hours for acute hamstring injuries in NFL players.Their results show an earlier return to play of 3 days forgrade 1 and 5 days for grade 2 injuries, with an overall1-game difference in the return to play. Most encourag-ingly, the authors noted a 0% recurrence rate comparedwith their baseline of 2 to 4 recurrences per year. Despitepromising results from level IV studies, as well as severalbasic science and animal studies that suggest PRP canenhance healing,5 there are no level I studies with ade-quate outcome measures and follow-up assessment thatprove its superiority. Several devices and systems areavailable for PRP preparation, with varying concentra-tions of growth factors, making comparisons between clin-ical studies difficult. Additionally, there is concern that, ifexcessive quantities of PRP are used, it may induce a floridfibrotic healing response in muscle tissues by increasingthe local concentration of TGF, based on data that TGFseems to be able to induce fibrosis in cultured muscle tis-sue.65 Therefore, at present, there is no evidence to recom-mend or discourage the adoption of PRP in clinicalpractice. Further research is required to standardize for-mulations (number of platelets and/or leukocytes) andadministration regimens, including volume of injection

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and timing of treatment, to optimize PRP application forthe management of muscle injuries.

Cell Therapy. Regenerative medicine involving tissueengineering and cell therapy has been directed towardskeletal muscle.1,14,33 Stem cells directly participate in tis-sue regeneration and thus influence muscle healing.39,76,82

After injury, patterns of growth factor expression deter-mine which cell types will participate in the wound healingprocess.76 High levels of TGF-b3 are related to the activa-tion of mesenchymal progenitor cells derived from trauma-tized muscle to promote wound healing after muscleinjury.67 On the other hand, high levels of TGF-b1 leadto muscle fibrosis by activating fibroblasts.39,82 Animalmodels of muscle injury have shown that muscle-derivedstem cells (MDSCs) improve both muscular struc-ture11,28,121 and muscle regeneration.12

Two potential techniques for skeletal muscle tissueengineering are in vitro and in vivo. With in vitro tissueengineering, stem cells from adult skeletal muscle areexpanded and seeded on a 3-dimensional (3D) scaffold.After the differentiation of stem cells, the neotissue graftcould be transplanted in the injured region. With in vivotissue engineering, the isolated MDSCs are seeded ona 3D scaffold carrier and immediately transplanted,obtaining direct delivery of stem cells in the musclelesion.103

At this time, the clinical use of stem cells is limited. Fur-ther research is necessary to identify the mechanismsinvolved in muscle regeneration to exactly understandthe therapeutic potential of stem cells.

Recurrence and Prevention. Prevention of hamstringinjuries is essential. Eccentric exercise is now emphasizedand produces greater strength gains than similar concen-tric hamstring movements.7,20,69,97 Improved hamstringstrength and endurance in a more functional position dur-ing sprinting increase the ability of the hamstrings toabsorb repeated eccentric loads before and during heelstrike. Identifying and correcting muscle imbalance andoptimizing neural timing along with progressive sprinttraining for identified high-risk athletes are advo-cated.48,87 Prevention strategies are likely most beneficialas part of a preseason training program. Athletes areencouraged to follow prevention programs and may complybecause the programs are closely associated with overallathletic performance.9,57

A few studies have investigated the effect of injury pre-vention programs on altering proposed risk factors forlower extremity injury.74,78 The injury prevention program‘‘The 11,’’ developed with the support of the FederationInternationale de Football Association (FIFA), aims toreduce the effect of intrinsic injury risk factors in soccer,and it has been validated in that sport.117,119 A successivemodified version of ‘‘The 11’’ (‘‘The 111’’) has been alsoshown to be effective in preventing injuries in youngfemale soccer players114 and elite male basketball play-ers.80 ‘‘The 111’’ provided more than a 40% reduction ininjury risk.114 Unfortunately, the program was not effec-tive in preventing the following injuries: ankle, anteriorthigh, posterior thigh (hamstrings), hip/groin, sprains,strains, fractures, or anterior lower leg pain (periostitis).

On the other hand, the program was effective in prevent-ing knee injuries, lower extremity injuries, overall injuries,severe injuries, and overuse injuries, such as lower extrem-ity tendon pain and low back pain. Therefore, the effective-ness of hamstring injury prevention programs remainscontroversial and deserves more attention.83-86

Treatment: Proximal Insertional Injuries

Essential to the treatment of proximal hamstring injuriesis the early recognition of the injury and timely referralto proper specialists. In general, nonoperative treatmentis considered for proximal hamstring injuries that involvea single tendon and/or multiple-tendon injuries with\2 cm of retraction. However, patient factors such as non-compliance, age, and activity level may influence treat-ment. Surgical indications for proximal hamstringinjuries include those involving 2 tendons with .2 cm ofretraction and 3-tendon tears. Identification and treatmentof surgical proximal hamstring injuries are best managedwithin 4 weeks, as later recognition provides for a more dif-ficult repair, leading to increased surgical complicationsand possibly inferior outcomes.35

Nonoperative Treatment. Single-tendon avulsions and 2-tendon tears with retraction \2 cm are treated nonopera-tively.34 Less active patients, those with medical comorbid-ities, and patients unable to comply with postoperativerehabilitation are also indications to manage these injuriesnonoperatively. Nonoperative management consists ofactivity modification, NSAIDs, and physical therapy.Other rehabilitation modalities include ultrasound, shock-wave therapy, electrical stimulation, and edema control.115

As the symptoms resolve, the core (abdominal), hip, andquadriceps may be added to a more aggressive programto prevent hamstring injuries.94 Pain can be a limitingfactor in the progression of rehabilitation. If patientsexperience difficulty with reintegration programs, anultrasound-guided corticosteroid injection can be used toprovide initial relief in up to 50% of patients at 4 weeks.133

An alternative to corticosteroid injections includes PRPperformed under computed tomography or ultrasoundguidance, which has similar outcomes to corticosteroid inexperienced hands. These injuries may take up to 6 weeksfor initial healing. In single-tendon tears, 6 weeks allowsthe tendon time to fibrose to the intact tendons, oftenallowing the initiation of limited activity. However, fullreturn to sport should only be allowed once the patient isasymptomatic with regard to pain and strength hasreturned to within 1 grade of the contralateral leg.95

In many tears managed nonoperatively, symptoms canpersist beyond the normal healing times. Knee flexionweakness and hip extension weakness often ensue monthsafter injury. Furthermore, a deformity in the area of theproximal hamstrings, difficulty in sitting, and scarring ofthe proximal hamstrings to the sciatic nerve can occur. Aserious complication of nonoperatively treated proximalhamstring injuries is hamstring syndrome, characterizedby local posterior buttock pain, discomfort over the ischialtuberosity during sitting, and worsening pain duringstretching and exercises that target the hamstrings.43

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These patients may benefit from surgical debridement andlate repair. In cases of recalcitrant hamstring syndrome,the sciatic nerve should be managed with surgical neurol-ysis, which has an 88% success rate in some series.102

Operative Treatment. Operative treatment for proximalhamstring tendon avulsions is recommended when 2 ten-dons are retracted �2 cm or for 3-tendon avulsions.34

Two-tendon injuries may often involve injury to a thirdhamstring muscle, either at the muscle belly or the muscu-lotendinous junction, that may not be seen on imagingstudies that are focused on proximal hamstring inser-tions.34 This possible third hamstring injury should betaken into consideration when deciding between operativeand nonoperative treatment in 2-tendon tears. Operativetreatment has high success rates and is also a considerationfor chronic injuries with complete or partial tears that failnonoperative management.16,29,43,105,107,127 However, moststudies indicated that the results of surgery for chronicruptures are inferior to acute repair.60,92

Surgical Procedure. The procedure involves placing thepatient prone on the operating room table with all bonyprominences well padded and the trunk in slight flexion(Figure 10). A transverse incision is made at the glutealcrease directly inferior to the ischial tuberosity (Figure11). Transverse incisions, in comparison to T-shaped orlongitudinal incisions, allow improved cosmesis and acces-sibility to avulsed tendons that insert along the coronalplane.43,70 The incision is deepened through the subcutane-ous fat to the gluteal fascia. Care must be taken to avoidthe posterior femoral cutaneous nerve. Once this nervousstructure is protected, a transverse incision is made in

the gluteal fascia. The gluteus maximus muscle is nextidentified and is elevated superiorly, or a split in one ofthe septae overlying the ischial tuberosity can be per-formed to expose the hamstring fascia.

Once the hamstring fascia is identified, a longitudinalincision is made through this fascia to locate the hamstringtendons. Often, these tendons are encased in scar tissueand erroneously appear to be intact. Care must be takento excise the overlying scar tissue, uncover the underlyinghematoma, and identify the injured hamstring tendons.The sciatic nerve is identified by palpation and can be pro-tected by retracting the tendons laterally (Figure 12). Thesciatic nerve is dissected free only in cases of chronic injurywith possible sciatic nerve scarring or possibly in cases inwhich the patient presents with sciatic nerve symptomspreoperatively.

The sciatic nerve is on average 1.2 cm lateral to themost lateral aspect of the ischial tuberosity.96 Once the sci-atic nerve has been safely protected, another layer offibrous tissue is often identified at the ends of each tendon.This fibrous tissue represents scarring of the tendons andshould be partially removed to allow for adequate healingof the tendons after repair. However, overzealous removalof this tissue could prevent adequate mobilization of theproximal hamstrings and produce shortened tendons.Once the tendons are mobilized, they are tagged withheavy suture before identifying and preparing the ischialtuberosity for tendon reattachment.

A periosteal elevator or a curette is used to clear off thelateral aspect of the ischial tuberosity to allow anatomicplacement of the hamstring tendons (Figure 13). The tuber-osity is then stimulated using manual instruments, allow-ing for a vascular bed for healing of the tendon origins to

Figure 10. Patient positioning for proximal hamstring repair.(A) Position of the table in slight flexion and (B) patientdraping.

Figure 11. Transverse incision with optional longitudinal limb(dotted line) for proximal hamstring surgical approach.

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the tuberosity. Motorized instruments are discouraged forthis portion of the surgery, as they can risk nerve injury.Some authors recommend making longitudinal scales inthe tuberosity using a small osteotome as a way to stimulatebiological healing. Suture anchors (2.4-mm BioCompositeSutureTak with No. 2 FiberWire, Arthrex Inc, Naples, Flor-ida) are then placed in an ‘‘X’’ configuration to repair thetendons to bone with a total of 5 anchors (Figure 14). Specialattention is paid to the anatomic location of the proximalhamstring tendons (Figure 15). The semimembranosus ten-don is the most lateral structure, with the confluent semi-tendinosus and long head of the biceps appearing moremedial. Regarding the footprint of the hamstring insertion,the semitendinosus and biceps femoris share an oval-shapedfootprint 2.7 cm long from proximal to distal and 1.8 cmwide from medial to lateral.96 The semimembranosus foot-print is crescent and lays lateral to the semitendinosusand biceps femoris footprint. It measures 3.1 cm from prox-imal to distal and 1.1 cm from medial to lateral.96

The sutures are placed through the tendon ends in a hor-izontal mattress pattern (from inferior to superior and tieddown from superior to inferior). The knee is flexed toapproximately 30�, while the tendons are tied down. The

fascia is closed, and the wound is closed in layers. Usingthe above technique, a 96% satisfaction rate and .75%recovery of strength have been documented.35

Patients with chronic ruptures who require operativetreatment may require an allograft bridge from theretracted tendon to the tuberosity. Reconstruction can beundertaken using an Achilles allograft with comparableresults to acute surgical repair.50

Postoperative Rehabilitation. Postoperative rehabilita-tion is an essential part of this surgery. To limit stress atthe surgery site, immediately after wound closure, theoperative leg is placed in a custom-fitted orthotic for thehip that restricts flexion of the hip from 30� to 40� (Figure16). Patients are prescribed aspirin for 4 weeks postopera-tively for deep vein thrombosis (DVT) prophylaxis,although the risk of DVT after a hamstring injury hasnot been firmly established. The first 10 to 14 days involvetoe-touch weightbearing with crutches. Weeks 2 to 5 con-sist of continued use of the hip orthotic and 25% weight-bearing. Passive range of motion of the hip with

Figure 12. Identification of the sciatic nerve with lateralretraction.

Figure 13. Surgical field with the ischial tuberosity exposed.Yellow dotted line shows the lateral aspect of the ischialtuberosity. (A) Skin markings. (B) Surgical field.

Figure 14. ‘‘X’’ configuration of sutures on the ischial tuber-osity. (A) Sutures through the tendon. (B) Final configuration.

Figure 15. Insertion of hamstring tendons on the ischialtuberosity.

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a therapist begins at 2 weeks, and active range of motionbegins at 4 weeks. At 6 weeks, the brace is discontinued,and the patient is allowed to fully bear weight and begingait training along with isotonic exercises. Also at 6 weeks,aqua therapy is introduced along with isotonic exercises,core strengthening, and closed chain exercises; range ofmotion is increased with caution for extreme ranges.Dynamic training and isometric strengthening begin at 8weeks after surgery, and at 10 weeks, an isometricstrength evaluation is performed with the knee at 60� offlexion. Sport-specific training and dry land training beginat 12 weeks. A fully isokinetic evaluation is performed at16 weeks at 60 deg/s, 120 deg/s, and 180 deg/s. Theseresults are compared with the contralateral leg. Fullreturn to sport is allowed once the operative leg is 80% ofthe nonoperative leg on isokinetic testing. Return to sportafter operative treatment, with accomplishment of theabove parameters, typically happens between 6 and 10months.15

Complications. Early complications most commonlyinvolve the sciatic nerve and include neurapraxia orstretch injury during surgery that eventually resolves.However, this can lead to burning pain radiating downthe leg and weakness of the distal operative extremityimmediately after surgery and in the first few weeks, mak-ing preoperative assessment of nerve symptoms essential.Other nerves that can be potentially harmed are the poste-rior femoral cutaneous nerve and the inferior glutealnerve, leading to dysesthesia and weakness of hip exten-sors, respectively. Nonneurogenic complications include

those mentioned for the late sequelae of nonoperativetreatment and comprise knee flexion weakness, hip exten-sion weakness, and deformity. Superficial and deep infec-tions can also occur and are a special concern for thissurgery because of the location of the surgical site and itsproximity to the gastrointestinal and genitourinary sys-tems. Other complications include the risk of reruptureand loss of strength.

Outcomes. Most series report that return of strengthranges from 60% to 90% of the contralateral leg, withmore than 95% reporting good to excellent subjectiveresults after surgical repair.15,23,29,43,70 In a series of 52patients, Cohen et al35 showed that 98% of patients weresatisfied with their outcome after surgery. Objective meas-ures such as the Lower Extremity Functional Scale andcustom Marx score showed a statistical difference betweenacute and chronic repairs, with acute repairs exhibitingimproved outcomes. However, patient questionnaire aver-ages did not show a statistical difference between acuteand chronic repairs. This indicates that injuries withdelayed diagnosis and failed nonoperative proximal ham-string injuries can still have favorable subjective patientoutcomes when treated with operative repair.35

Treatment: Distal Insertional Injuries

The distal attachment of the biceps femoris is most com-monly injured with a varus hyperextension mechanismas part of multiligament knee injuries.44,52,72,91 An isolateddistal semimembranosus avulsion is rare.4 In contrast, iso-lated distal semitendinosus tendon avulsions are becomingmore recognized38,109,110 but can be misdiagnosed as adistal-third muscle belly hamstring injury. An MRI scanof the thigh and knee over the full course of the semitendi-nosus tendon can confirm the diagnosis (Figure 17). Distalsemitendinosus tendon avulsions cause much more timeloss from sports than hamstring muscle belly injuries onaverage. Cooper and Conway38 reported a case series of 25distal semitendinosus tendon ruptures in high-level ath-letes. Early treatment always involved nonoperative treat-ment, including rest, modalities, and rehabilitation

Figure 16. Postoperative brace with the hip placed in 30� to40� of flexion.

Figure 17. Axial magnetic resonance imaging scan demon-strating a distal semitendinosus tear. (A) Distally at the semi-tendinosus insertion (*), showing fluid signal intensity withinthe expected course of the tendon sheath (arrowhead), and(B) proximally at the retracted tendon stump (arrow).

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exercises, followed by functional progression. Forty-two per-cent failed initial nonoperative treatment and subsequentlyhad surgery with resection of the torn tendon and adjacentscar tissue, with an average recovery time of 12.8 weeks.Another group of patients were treated with acute surgerythat resected the torn tendon and adjacent scar tissuewithin 4 weeks of injury. The acute-phase group had anaverage recovery of 6.8 weeks after surgery. The authorsconcluded that distal semitendinosus ruptures frequentlydo not recover when treated nonoperatively. Therefore,acute surgery may be considered in elite athletes forwhom time to recovery is very important for more favorabletime frames to return to participation. Further indicationsfor immediate surgery are the presence of a painful mass,inability to walk well with a normal gait pattern, or inabilityto extend the knee fully.79

SUMMARY

Hamstring injuries occur in athletes of all ages, all types ofsport, and all levels of competition. Most often, a detailedhistory, a thorough physical examination, and a completereview of the imaging studies will confirm the presenceof a hamstring injury. Clinical grading, traditional radio-graphic grading, and a novel MRI scoring system mayallow a more precise prediction of return to sport. Surgeryis indicated for certain proximal and distal avulsion inju-ries. Nonoperative treatment of midsubstance injuriesmay include biological treatment in the future. Preventionstrategies will also be beneficial.

An online CME course associated with this article isavailable for 1 AMA PRA Category 1 CreditTM at http://ajsm-cme.sagepub.com. In accordance with the standardsof the Accreditation Council for Continuing Medical Edu-cation (ACCME), it is the policy of The American Ortho-paedic Society for Sports Medicine that authors, editors,and planners disclose to the learners all financial rela-tionships during the past 12 months with any commercialinterest (A ‘commercial interest’ is any entity producing,marketing, re-selling, or distributing health care goodsor services consumed by, or used on, patients). Any andall disclosures are provided in the online journal CMEarea which is provided to all participants before theyactually take the CME activity. In accordance withAOSSM policy, authors, editors, and planners’ participa-tion in this educational activity will be predicated upontimely submission and review of AOSSM disclosure. Non-compliance will result in an author/editor or planner to bestricken from participating in this CME activity.

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