M u s c u l o s k e l e t a l I m a g i n g • R ev i ew Rubin Hamstring Injuries

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Musculoskeletal Imaging Review

David A. Rubin1 Rubin DA

Imaging Diagnosis and Prognostication of Hamstring Injuries OBJECTIVE. Hamstring injuries are common in sports. Although management and outcomes are sport specific, clinical evaluation alone is a poor guide for treatment planning and prognostication. Cross-sectional imaging has added value in these cases. CONCLUSION. Specifically, the location (tendon attachment, classic or intramuscular myotendinous junction, or extramuscular portion of the tendon), specific muscles involved, and anatomic extent are factors that can influence the immediate treatment, expected convalescent period, and risk of recurrence in these athletes.

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Keywords: avulsion, hamstring, injury, muscle, strain DOI:10.2214/AJR.12.8784 Received February 21, 2012; accepted after revision March 22, 2012. 1

Mallinckrodt Institute of Radiology, 510 S Kingshighway, St. Louis, MO 63110. Address correspondence to D. A. Rubin ([email protected]).

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uscle injuries account for up to half of all injuries in some sports and are a common reason for lost playing time [1–3]. In recreational athletes, management is not critical, because most injuries heal spontaneously. However, in high-end performers, a precise timely diagnosis is necessary. MRI or, in some cases, ultrasound can help the treating clinician optimize initial treatment and plan convalescence and rehabilitation to minimize the impact on the player’s and team’s well-being. A muscle contusion or bruise (sometimes called a “Charlie horse”) results from direct trauma. The quadriceps muscles are at highest risk because they are located anteriorly and are relatively exposed. Petechial hemorrhage and swelling occurs within the muscle belly, centered where an external force either directly injured the muscle or crushed it against the underlying bone. Muscle contusions heal with conservative management, and athletes can typically return to activity within a week. In severe cases, an intramuscular hematoma may form, delaying recovery. Hematomas usually resolve spontaneously but occasionally lead to seromas or myositis ossificans [4, 5]. Indirect trauma causes most sports-related muscle injuries. These noncontact injuries are due to eccentric stretching, which occurs when a muscle contracts at the same time that it is being lengthened [2]. Although a single violent stretch can avulse a tendon from its bone anchor, most commonly a stretching injury will produce a muscle strain or “pulled” muscle [6]. A strain is characterized by tear-

ing of fibers in the muscle-tendon unit, which may be either microscopic or macroscopic. Muscles that act eccentrically, that cross two joints, and that contain a large proportion of type 2 fast-twitch fibers are at greatest risk [7]. Strains take longer to heal compared with muscle contusions [8], but the amount of time a player may lose from training and competition is highly variable. Depending on the specific sport (and, in team sports, the position played), the muscles involved, the severity of the injury, and the location of damage within the muscle-tendon unit, an athlete may be out anywhere from a few days to a year or more. In addition, returning to competition too soon risks recurrent injury. Muscle injuries account for a large amount of lost player time, potentially affecting both athletes’ careers and teams’ competitiveness. Thus, team doctors are keenly interested in optimizing treatment and accurately prognosticating the length of convalescence following these injuries [9]. The hamstrings are the powerful posterior thigh muscles that extend the hip and flex the knee. In many sports, this muscle group accounts for the most injuries and lost player days [3]. Contusions to the hamstrings are rare, so most injuries are either muscle strains or tendon avulsions. For strains and avulsions, physical examination is a relatively poor guide to management and a weak predictor of injury recovery times. In this review, I will emphasize circumstances in which imaging studies can supplement clinical evaluation to direct treatment of hamstring trauma. A second major topic

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Rubin will be the use of radiologic studies as an aid to predicting the time until a player can return to sports. Most of the research in these two areas has been done with MRI, which I will emphasize. Where appropriate, I will also present data from ultrasound studies. Before discussing the imaging features of hamstring injuries, a brief review of the relevant anatomy and an overview of the pertinent clinical issues are in order. Relevant Anatomy The semimembranosus, semitendinosus, and biceps femoris form the hamstring group. The proximal tendons of the semitendinosus and long head of the biceps femoris merge to form a conjoint tendon, which takes its origin from the inferomedial facet of the ischial tuberosity; the semitendinosus also has a secondary muscular origin from the inferior ischium [10]. The short head of the biceps femoris has a muscular origin along the linea aspera of the posterior femur [11]. A long proximal tendon of the semimembranosus originates from the superolateral facet of the ischial tuberosity, slightly anterolateral and cranial to the conjoint tendon origin [12, 13]. The proximal semimembranosus tendon is approximately twice the diameter of the conjoint tendon [10]. The two heads of the biceps femoris compose the lateral hamstring muscle group and distally give rise to a tendon that merges with the fibular collateral ligament of the knee to insert on the lateral aspect of the fibular head. A second smaller tendon slip inserts on the proximal lateral tibia [11]. Distally, the semimembranosus has a central tendon insertion on the medial proximal tibia and at least four minor tendon slips attached to various supporting soft-tissue structures of the knee [13]. The semitendinosus muscle, which, together with the semimembranosus forms the medial hamstring group, terminates in a very long tendon. The tendon passes superficially to the knee’s medial collateral ligament and inserts on the anteromedial proximal tibia [11], forming the pes anserinus with the distal sartorius and gracilis tendons. The hamstring’s tendons originate deep within the muscle bellies, running nearly the length of the muscles before emerging from the muscle ends [14]. Within the muscle bellies, the muscle fibers converge in a pennate arrangement onto these central tendons. In addition, each of the three hamstring muscles is surrounded by an aponeurotic fibrous covering. Thus, there are three distinct interfaces where tissues of different physical properties

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meet: first, the intramuscular myotendinous junction centrally running along the long axis of each muscle; second, the classic myotendinous junctions, where the proximal and distal tendons emerge from the muscle belly; and third, the myofascial junction in the muscle periphery. Each of these interfaces is susceptible to eccentric injuries [10, 15, 16]. The injuries that occur in these three distributions—as well as those involving the extramuscular portion of the tendons and the tendon-bone interfaces— are relatively unique in their inciting activities and clinical presentations. Most important, injury outcomes may differ depending on which part of the muscle-tendon-bone unit is involved. On clinical examination, it may not be possible to determine where a given injury is centered. One of the advantages of imaging is the ability to directly show the distribution (and extent) of hamstring muscle strains. Clinical Diagnosis, Management, and Outcomes Hamstring Avulsions Avulsions of the hamstring attachments are much less common than muscle strains, and distal avulsions are particularly uncommon as isolated injuries [17]. Avulsions of the proximal hamstring tendons from the ischial tuberosity affect the conjoint tendon more frequently than the biceps femoris tendon alone; avulsions of the semimembranosus origin are rare [17]. Waterskiing accounts for a large number of these injuries [18]. A common injury mechanism is a sudden pull by the boat, resulting in violent flexion at the hips at the same time that the knees are locked in full extension. Other causes of proximal avulsions are activities where splits are commonly performed, such as ballet and gymnastics [12]. Complete injuries with or without tendon retraction are more common than partial tears [12], and most authors advocate immediate surgery for complete avulsions [10, 17, 19]. Patients who are treated conservatively and for whom treatment fails can still undergo delayed repair [18], but this often means a more difficult operation and poorer outcomes [12]. Recovery times range from 3 to 18 months [18], with 80% of athletes treated surgically able to return to sports within 6 months [12]. Typical Hamstring Strains Classic hamstring strains result from rapid accelerations, decelerations, and changes in direction [9], in such sports as track-andfield, soccer, and American football [3, 16,

20]. Prior lower extremity trauma, older age, and deconditioning are contributory risk factors in some studies [3, 20–23]. Regardless of the sport, the long head of the biceps femoris is by far the most commonly strained muscle [15–17, 23–25]. Most large series identify the semimembranosus as the second most commonly affected in single-muscle injuries [17, 25]. More than one muscle is involved in approximately one third of cases, typically the long head of the biceps combined with the semitendinosus or with the short head of the biceps [15, 24]. Strains most commonly involve the proximal myotendinous junction, followed in frequency by the intramuscular myotendinous junction, the distal myotendinous junction, and finally the myofascial junction [16]. Athletes experience a sudden sharp pain in the back of the thigh, sometimes with an audible “pop.” The injury usually precludes further activity. Examination reveals focal tenderness; in severe cases when there is actual fiber disruption, a palpable defect or visible bruising may be evident. Initial treatment of muscle strains follows the “PRICE” principle: protection, rest, ice, compression, and elevation. Analgesics or nonsteroidal antiinflammatory drugs are used for pain control [2, 26]. A program of early mobilization, stretching, and flexibility training is then instituted, with gradual introduction of more sport-specific activities [27]. Ideally, players will not return to play if there is a persistent muscle strength deficit (compared with the contralateral side), but the decision is usually predicated on functional testing [9]. Premature return may predispose to repeat hamstring or other injuries [2, 27]. There are advocates for aspirating intramuscular hematomas (after they liquefy) when they complicate muscle injuries, but the data supporting this intervention are anecdotal [28, 29]. Similarly, the role of intramuscular (or peritendinous) steroid or platelet-rich plasma injections to speed healing is uncertain, with largely uncontrolled unblinded studies reporting their use [28, 30, 31]. To my knowledge, there are no controlled studies investigating when it is safe for an athlete to return to training or competition. Typically, players in team sports can compete at an effective level earlier than those in individual sports. After all, if one member of a soccer team is only playing at 85% of full capacity, the team may still be very competitive overall, but for a sprinter in an event where races are decided by tenths of a second, even run-

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Hamstring Injuries

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Fig. 1—52-year-old man with proximal hamstring avulsion resulting from waterskiing injury 4 weeks previously. A, Coronal STIR image shows complete tear of left conjoint tendon origin (black arrow) and intact right tendon origin (white arrows). There is mild distal tendon retraction. B, Transverse T1-weighted image shows torn tendon stump (long arrow) separate from sciatic nerve (short arrow), which is surrounded by fat. Because of small amount of retraction and normal sciatic nerve, injury was managed nonoperatively and healed.

ning at 95% of his capacity may mean the difference between first and last place. So in sports such as soccer and American football, the mean time to return to play is 2 weeks [3, 20], while for elite sprinters the average is

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16 weeks, eight times longer [24]. However, within each sport, there is a very wide range of recuperation times (e.g., 1–128 days in professional soccer players) [3]. Importantly, the clinical severity of the initial injury cannot predict the expected recovery time [24]. In addition, there does not seem to be a relationship between which muscle is injured and healing time [25]. In general, the injured part of the muscle-tendon unit does not predict return to play [23], with one important exception: in high-performance sprinters, proximal biceps femoris strains may extend proximally

to involve the free tendon, and, in these cases, recovery takes, on average, three times longer (35 weeks vs 12 weeks when only the proximal myotendinous junction is injured) [24]. However, it is not possible to tell whether the injury extends into the proximal tendon by palpation alone. Traditional clinical grading of muscle injuries (grade 0, no findings; grade 1, focal tenderness without loss in strength; grade 2, loss in strength presumably indicating partial fiber disruption; and grade 3, loss in function indicating complete fiber disruption) also does

Fig. 2—48-year-old woman with acute proximal hamstring avulsion. A, Coronal STIR image shows severe distal retraction of torn hamstring tendons (arrow), with large surrounding hematoma. B, Transverse T1-weighted image through ischial tuberosity shows complete tendon avulsions on right. On left, note normal semimembranosus tendon (long black arrow), normal conjoint tendon (short black arrow), and sciatic nerve (white arrow). C, Transverse fat-suppressed T2-weighted image through proximal thigh shows large hematoma enveloping distally retracted semimembranosus tendon (black arrow) and sciatic nerve (white arrow). At time of surgical repair, torn tendons were scarred to sciatic nerve.

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Rubin

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Fig. 3—30-year-old man, offensive lineman on professional football team, with grade 1 central myotendinous biceps femoris strain. A, Transverse fat-suppressed T2-weighted image shows intramuscular edema surrounding long-head biceps femoris central tendon (arrow) and in deep fascia. Approximately 50% of muscle cross-section is involved. B, Coronal STIR image shows typical feathery edema in bipennate muscle fibers (arrows) converging on central tendon.

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Fig. 4—27-year-old man, offensive guard on professional football team, with grade 1 peripheral (myofascial) biceps femoris strain. A and B, Transverse T1-weighted (A) and fat-suppressed T2-weighted (B) images of thigh show edema confined to lateral margin of long-head biceps femoris muscle (arrow, B) involving approximately 10% of muscle cross-section. C, Coronal STIR image shows extent of injury at lateral myofascial junction (arrows). Compare with Fig. 3.

a poor job of predicting recovery times. The measured loss of active knee extension is correlated with return to play [16, 32]. However, even clinical grading systems that incorporate this measure can provide only rough estimates of recovery times. For example, in Australian football, players with clinical grade 1 hamstring strains average 9 days until they can return to competition, whereas those with grade 2 injuries average 27 days; however, the ranges of recovery times overlap greatly (5–35 days for grade 1 and 4–56 days for grade 2 strains) [33]. Recurrent hamstring strains in the same season occur commonly, with rates ranging from 16% in soccer and American football [3, 20] up to 34% in Australian football [7].

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C In most studies, athletes take longer to return to play after a recurrence compared with the initial injury [3, 25]. There are few, if any, clinical clues that can predict a second injury. In one study of track and field athletes, those whose initial strains were less severe (defined by < 20° loss of active knee extension) paradoxically had higher 2-year recurrence rates compared with athletes whose initial injuries were more severe [32].

Atypical (Stretching) Hamstring Strains Recently, a different type of hamstring strain has been identified. The mechanism is excessive stretching combined with hip flexion and knee extension, as opposed to rapid cutting maneuvers. Initial reports described professional dancers injured during slow stretching [34]. However, it is now clear that these injuries can occur in any activity involving excessive stretch of the hamstrings, whether that

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Hamstring Injuries

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Fig. 5—23-year-old man with grade 1 distal myotendinous hamstring strain. A, Sagittal fat-suppressed fast spin-echo image shows edema centered between distal muscle belly (black arrow) and tendon (white arrow) of semitendinosus. B, Transverse fat-suppressed T2-weighted image shows involvement of entire cross-section of distal muscle (arrow).

occurs quickly or slowly [35]. Examples include sports with high kicking (soccer, martial arts, and dance) or front splits (rhythmic gymnastics, cheerleading, and aerobics). These atypical hamstring injuries differ from the more common classic strains in several important ways. First, the initial symptoms may be relatively mild, with some athletes able to finish their activity after the acute injury [34]. Women are affected more than men are [35]. The injuries all occur very close to the ischial tuberosity, and, contrary to the case for typical strains, they primarily involve the semimembranosus. Other muscles may also be affected, often in combination with the semimembranosus, including the quadratus femoris, adductor magnus, and semitendinosus. Furthermore, in the semimembranosus, the injury extends into the portion of the proximal tendon that is not surrounded by the muscle (i.e., the free tendon). Finally, these injuries take much longer to heal, with a mean recovery time of 50 weeks in dancers and 31 weeks in other athletes [34, 35]. In one report, 47% of these atypical hamstring strains were career ending [35]. Imaging Diagnosis, Treatment Guidance, and Prognostication For suspected proximal tendon avulsions, the role of imaging is twofold. First, it may be impossible to determine with physical examination alone whether a strain or tendon avulsion is present, with the latter typically requiring immediate surgery [12, 17, 19].

Fractures, proximal hamstring tendinopathy, ischial bursitis, ischiofemoral impingement, and iliopsoas tendinitis can also potentially mimic a proximal tendon avulsion, and these conditions are easily identified with MRI [36, 37]. Second, once a diagnosis of an avulsed tendon is made, imaging is typically used to guide treatment planning. The key observations to note are whether the conjoint tendon, the semimembranosus tendon, or both are involved and whether the tear is partial or full thickness (Fig. 1). For fullthickness tears, the amount of distal tendon retraction, the degree of underlying tendinopathy, and the relationship of the torn tendon ends to the sciatic nerve (Fig. 2) influence treatment planning [12, 17, 18]. Muscle strains have a characteristic appearance on cross-sectional images. Sonographically, there is disruption of the normally organized echogenic fibrillar muscle pattern [16]. Hypoechoic or anechoic clefts may be present in the muscle substance or tracking around the periphery of the injured muscle [38]. A macroscopic hematoma will typically appear as a focal mass in or between the muscles, with echotexture varying depending on the age and amount of internal liquefaction. On MRI, the most common finding is high-signal-intensity edema and hemorrhage (on water-sensitive sequences) centered at the main myotendinous junction, surrounding the intramuscular part of the tendon, or in the periphery of the muscle at the myofascial junction [10, 16, 38, 39] (Figs.

3–5). Corresponding to the clinical grading scheme, on MRI, a grade 1 injury is present when all the myotendinous fibers are intact, even if they are distorted. Associated edema extending into the muscle belly or deep fascia is common and may be extensive, but the injury remains grade 1 as long as there are no gaps within the muscle fibers [7, 40] (Figs. 3–5). More severe (grade 2) injuries result in macroscopic fiber disruption, often with loss of the normally low-signal-intensity intramuscular tendon on T1-weighted images [16, 41]. An intramuscular hematoma may form within the space vacated by the disrupted fibers in a grade 2 injury. Hematomas will focally enlarge the affected compartment and will contain subacute or chronic blood products on T1-weighted images [42] (Fig. 6). Grade 3 strains are rare and represent complete disruption of the entire myotendinous cross-section. Because the extent of the injury carries prognostic significance, the imaging study should include the entirety of the abnormality, when possible. In addition to localizing the injury, the radiologist should also estimate the length of the edematous tissues and the maximum amount of muscle crosssection that is affected. I find that, in difficult cases (as in very muscular athletes with little intermuscular fat), including the contralateral thigh in the imaging volume can be helpful to identify the normal anatomic boundaries. It is important to recognize that some clinically diagnosed hamstring strains will have no ultrasound or MRI findings (Fig. 7). MRI-

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Rubin

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B Fig. 6—18-year-old man with grade 2 biceps femoris strain. A, Coronal STIR image shows high-signal-intensity gaps between muscle fibers. B, Transverse T1-weighted image shows hyperintense subacute hematoma (arrow) in biceps femoris muscle. C, Sagittal STIR image through left thigh shows extent of intramuscular hematoma. Aspiration of hematoma was performed under ultrasound guidance once it had liquefied.

C and ultrasound-negative cases account for up to 45% of clinically suspected injuries [7, 16, 33]. It is unclear whether these cases represent minor hamstring injuries whose manifestations fall below the threshold needed for an imaging diagnosis or whether they are injuries to the spine or trunk with pain referred to the posterior thigh [7, 25]. Regardless of the explanation, the players who have no imaging findings have better prognoses and shorter convalescent times compared with those with positive imaging studies [7, 16, 23, 33]. Although the initial management of most hamstring strains is conservative, in rare cas-

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es, a complete separation of all muscle fibers from the tendon can occur (i.e., a grade 3 injury) and, in selected athletes, may be repaired surgically. More commonly, a grade 2 injury that partly disrupts the myotendinous fibers will result in an intermuscular or intramuscular hematoma (Fig. 6). Hematomas between the muscles tend to rapidly dissipate and resorb [10]. However, some practitioners think that aspirating a large intramuscular hematoma will speed healing by bringing the torn fibers into closer apposition [10, 28, 29]. For these players, MRI or ultrasound is needed to establish that a hematoma has liquefied before aspiration can be contemplated. In many instances, ultrasound will also be used to guide needle placement for the aspiration, as well as for the potential injection of steroid or other agents. Ultrasound-guided peritendinous steroid injection has also been advocated to provide symptomatic relief in patients with the atypical stretching proximal hamstring injuries that involve the proximal free tendon [31]. Imaging plays a bigger role in prognostication after hamstring strains. First, crosssectional images can distinguish proximal hamstring injuries of the stretching variety from typical strains, for athletes for whom the injury mechanism is not clear clinically. MRI showing injury to the semimembranosus proximal myotendinous junction or the proximal free tendon (Fig. 8) indicates a stretching injury and predicts a prolonged recovery time, typically 6–24 months [34,

35]. An injury localized to the long-head biceps femoris alone or combined with other muscles is characteristic of a typical hamstring strain, with a return to play in a matter of weeks. Second, in explosive sports such as sprinting, the proximity of a long-head biceps femoris injury to the ischial tuberosity and the length of the edematous muscle measured on MRI relates to the expected time missed from training (Fig. 9). In one study, sprinters with MRI examinations showing involvement of the proximal extramuscular part of the biceps tendon were out from their sport for an average of 35 weeks, compared with only 12 weeks for those whose injuries involved only the myotendinous junction or intramuscular tendon [24]. Other than injuries that involve the free tendons, the location of the insult within the myotendinous unit does not seem to have prognostic significance for hamstring injuries. Injuries to the central myotendinous junction behave similarly to those at the proximal and distal myotendinous junctions [43]. Interestingly, in rectus femoris strains, those that occur in the periphery at the myofascial junction recover much more quickly than those surrounding the central tendon, with an average return to play of 9 versus 27 days [44]. The same relationship does not appear to hold for hamstring strains [38]. However, in both the quadriceps and hamstring muscles, injuries that are clinically thought to be strains but that have no imaging findings (Fig. 7) universally recover faster than those with

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Hamstring Injuries

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Fig. 7—24-year-old man, wide receiver on professional football team, with clinically suspected right hamstring strain. A and B, Transverse T1-weighted (A) and fat-suppressed T2-weighted (B) images through thighs show no abnormality on symptomatic right side. Skin marker (white arrows) indicates area of tenderness. Note mild residual edema in left semitendinosus muscle adjacent to low-signal-intensity scar (black arrows) from strain earlier in season. He was able to return to play week following right thigh injury and negative MRI.

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Fig. 8—33-year-old male elite marathon runner with proximal hamstring strain sustained during prerace stretching. A, Transverse fat-suppressed T2-weighted image through proximal thigh shows edema throughout semimembranosus muscle, with surrounding fascial edema. B, Transverse fat-suppressed T2-weighted image more proximally, at level of ischial tuberosities, shows extension of injury surrounding proximal free tendon (arrow). There was no tendon avulsion. Injury of semimembranosus and involvement of free tendon is characteristic of stretch-induced injury and portends very lengthy recovery. At last follow-up, patient was still unable to run after 6 months of rest.

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Fig. 9—28-year-old man, professional baseball pitcher, with proximal hamstring strain. A, Transverse fat-suppressed T2-weighted image through mid thigh shows edema involving more than 50% of cross-sectional area of biceps femoris muscle. B, More proximally, injury extends into proximal-most aspect of muscle (arrow). C, Coronal STIR image shows proximal extent of tear, extending almost to level of ischial tuberosity (arrow). In sprinting athletes, injuries close to ischium take longer to heal. This player was able to return to pitching in 2.5 weeks.

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Rubin positive imaging studies, often in one half or one third of the time [3, 7, 16, 23, 33, 38, 44]. In addition, in the hamstrings, both the length and cross-section of the muscle edema correlate with recovery times, even for injuries that have similar clinical findings and initial severity [3, 7, 43, 45]. For example, one study showed that injuries took longer than 6 weeks to heal when the maximum crosssection area of edematous muscle measured greater than 50% on MRI [10]. In addition, imaging evidence of macroscopic fiber disruption (a grade 2 or 3 strain)—manifest by either architectural distortion or the presence of an intramuscular hematoma—portends a longer recovery time compared with a (grade 1) hamstring injury with completely intact fibers [16, 25]. Currently, the final decision of when an athlete is able to return to play is based on clinical assessment, not follow-up imaging studies. However, there may be information available on imaging studies that complements the clinical assessment. For example, in one study of elite sprinters, persistent MRI findings were often present in athletes who thought they were not ready to return to competition, even when their objective clinical assessments showed they had regained greater than 90% of their strength and flexibility [24]. On the other hand, in Australian football, 20–35% of athletes had persistent MRI or ultrasound findings 6 weeks after their injuries, although almost all had returned to competition by that time [38]. To my knowledge, there have been no investigations trying to incorporate findings on follow-up imaging studies into the decision to release an athlete for sport. One final issue is whether there are imaging features that can help predict recurrent injuries. Most hamstring injuries will heal with a variable amount of scar tissue (Fig. 7), and the player will be able to regain their former level of performance. However, injury to the same thigh will reoccur in the same or next season in approximately 15% of those injured [7, 25, 32]. In Australian football players, the length of the initial injury on MRI is associated with the risk of a second hamstring strain in the same season, with a 33% recurrence risk if the original extent of muscle edema is greater than 6 cm long, but only 7% otherwise [39]. Players with MRI-negative injuries have virtually no increased risk of recurrence [7, 39]. References 1. Bass AL. Injuries of the leg in football and ballet. Proc R Soc Med 1967; 60:527–530

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