Returning an athlete to competition following muscle injury can be one of the most challenging tasks for the sports medicine team. Injury recurrence is high, particularly when returning to sport within the same competitive season. Prediction of time loss from injury as well as those who are at risk of reinjury has proven challenging. Multiple studies have evaluated both clinical tests and imaging findings (predominately magnetic resonance imaging [MRI]) to assist with prognosis and return to play, but there is no agreement regarding optimal return to play protocol or utilization of imaging. More telling is the fact that injury rates have not decreased. Ultrasound has become an increasingly utilized imaging modality which offers several potential advantages over MRI and may help to identify those athletes at risk of reinjury who otherwise pass current functional clinical testing. Our clinical experience has found the addition of serial ultrasound examination a valuable tool in stratifying risk and providing guidance on return to play.
Epidemiology of Muscle Injury in Sport
Muscle injuries comprise 33% to nearly 50% of total injuries in high-demand sports such as soccer, American football, and track & field (1–5). Greater than 50% of these muscle injuries involve the thigh, with the hamstring muscle group being the most commonly involved (1–4). One of the most difficult challenges associated with these injuries is the high rate of recurrence. The recurrence rate for hamstring strain injuries has been reported between 12% and 33% with quadriceps strain recurrence slightly less at 7% to 20% (6–8). Greater than 50% of recurrent hamstring injuries occur within 1 month after return to play from the initial injury, demonstrating the challenge of safely returning these athletes to sport within the same competitive season (8). Little progress has been made in reducing the burden of these injuries. In fact, the rate of hamstring injuries was shown to have increased by 4% annually in a cohort of professional men’s soccer players (9). Hamstring injuries alone have been reported to average 90 d of time loss per club per season in professional soccer (5). It also is difficult to understand the full spectrum of injury severity given confusion regarding a standard injury grading system (3,5,10,11).
Ultrasound Evaluation of Muscle Injury
As with other areas of musculoskeletal imaging in sports medicine, ultrasound has shown to be an accurate modality to identify and characterize muscle injury (12–14). Prior to MRI, ultrasound was the first imaging modality available to evaluate muscle pathology (13). However, review of recent literature involving sports-related muscle injury demonstrates a predominance of MRI related studies. Although MRI is quite sensitive for muscle injury, ultrasound evaluation provides several potential advantages that have not been fully borne out in the literature. The interactive nature of ultrasound, especially when performed by the treating team physician, allows for clinical correlation at the time of examination, likely increasing the sensitivity for subtle pathology. Also, this aids in interpretation of chronic findings of fibrosis which may be asymptomatic and not clinically relevant. The ability to perform treatment, such as hematoma evacuation, at the time of evaluation improves efficiency by decreasing the need for multiple appointments.
However, we would argue that the primary advantage of ultrasound over MRI in evaluation of muscle injury is the ability to perform serial examinations to monitor healing and aid in return to play decision making. The increasing availability of ultrasound coupled with its relatively low cost and ease of use make serial examination feasible. Multiple follow up ultrasound studies will still likely be cost effective compared with a single MRI at many institutions. Our preliminary experience has found two unique aspects of ultrasound imaging to be quite helpful in assessing the healing muscle injury: Doppler and dynamic evaluation of muscle contraction. Doppler evaluation has become standard practice in sonographic evaluation of tendon disorders where it is able to demonstrate the neovascularity of tendinosis. It has received much less attention in relation to muscle injury, but has been suggested as a potential way to monitor healing of an acute muscle injury or “reactivation” of chronic fibrotic scar tissue (15). Increased blood flow on Doppler imaging, or hyperemia, at the site of muscle injury will be seen within the first few days after injury. This hyperemia will consolidate and decrease over time and can be thought of as a surrogate of active healing within the lesion (Fig. 1). Ongoing hyperemia may suggest that healing has not reached adequate strength and convey an increased risk of recurrent injury. Our experience has shown significant changes can be appreciated over a relative short period of time (i.e., 1-2 wk) and can be helpful in identifying lesions which are clinically improved, but potentially at high risk of recurrent injury (Fig. 1A–C). Hyperemia also can be useful in evaluating reactivation of chronic fibrotic scar tissue. Fibrotic scar is represented as a hyperechoic region within the muscle (Fig. 1D). Hyperemia about a region of chronic fibrosis (Fig. 1E) can aid in identification of subtle pathology where the scar and surrounding tissue has become aggravated without new muscle fiber disruption. Symptoms can be correlated with the location of fibrotic scar tissue to further support the diagnosis.
Dynamic evaluation with muscle contraction is another key component in the ultrasound evaluation of muscle healing. Initially, a region of significant muscle fiber disruption will demonstrate free muscle fibers floating in anechoic traumatic hemorrhagic fluid (Fig. 2) and dynamic evaluation will fail to show any contraction across the lesion. Over time, the hematoma will organize, becoming hyperechoic as the free fluid is absorbed and muscle fibers will begin to reinsert. Serial dynamic examination will demonstrate restoration of functional contractile properties across the zone of injury. There may be persistent deformity if the fascia has been disrupted, but functional contraction should still be appreciated across the healed lesion. There is concern that if contraction has not been restored, the adjacent muscle is at risk of further injury with potential of more serious extension across fibroaponeurotic tissue planes or the so called “intramuscular” or “central tendon” disruption.
Predicting Return to Play
Multiple attempts have been made to predict return to play following thigh muscle strain injury, but currently no well validated protocol exists. The lack of consensus regarding definition of “return to play” as well as lack of clear validated criteria further complicates the matter (8). Several clinical factors have been associated with prolonged return to play including presence of a structural injury, stretch type injury mechanism, increased pain, and delayed presentation (16–18). However, it is difficult to stratify this group, particularly with regards to determining the risk of recurrent injury. It would seem reasonable that imaging could add additional information to help guide prognosis. Multiple studies have evaluated the efficacy of MRI in predicting time to return to play as well as determining reinjury risk with mixed results (1,11,12,19–31). A recent systematic review by van Heumen and colleagues concluded that there is no strong evidence for any MRI finding at baseline and/or return to play in predicting hamstring reinjury risk (28). To our knowledge, only one study has evaluated ultrasound assessment of muscle injury (hamstring) in regards to predicting return to play (12). They found that ultrasound was equivalent to MRI in assessment of acute hamstring injury, but that MRI was more sensitive for follow-up imaging. However, only static grayscale ultrasound images were obtained.
Ultrasound Return to Play Protocol
While factors associated with location and extent of initial muscle injury are undoubtedly important in predicting return to play, they provide no information regarding the quality and extent of the healing muscle over time. Multiple factors are involved in an athlete’s return to play from muscle injury and athletes will heal at different rates irrespective of type and location of injury. Ultrasound has the unique ability to evaluate aspects of muscle healing that have not been systematically studied to date (e.g., hyperemia and contraction). Ultrasound offers higher spatial resolution than MRI in addition to its dynamic capabilities. Our clinical experience suggests that serial ultrasound evaluations of thigh muscle injury may be able to reduce the recurrence rate of both hamstring and quadriceps muscle strains and allow for a standardized return to play criteria. The protocol currently used at the University of Iowa as part of our multidisciplinary approach to return to play following muscle injury is presented in Table 1.
Timing of the Ultrasound Examination
Consideration should be given to timing of the initial examination. The ideal timing of examination after injury has not been systematically studied, but between 2 and 48 h has been suggested and our experience would support this recommendation (13). If the examination is performed too early postinjury then the hematoma has not had adequate time to fully form and there may be a risk of false negative examination, or underappreciation of the severity of the injury. Forty-eight hours appears to be a practical guideline as this allows time for athletes to travel home from away competitions and/or be seen in the office after weekend competitions if on-site ultrasound capabilities are not available.
Technical Aspects of the Ultrasound Evaluation
A mid to high frequency (e.g., 12–5 MHz) linear array transducer should be used if possible to ensure adequate resolution and sensitivity for subtle pathology. There may be cases in large well-muscled athletes where a lower frequency (e.g., 5–1 MHz) curvilinear array transducer may be required for complete evaluation; however, the majority of strain injuries occur in the more superficial muscle layers (in contradistinction to contusive injuries) and are typically well visualized with a linear array transducer. Extended field of view imaging (if available) can be useful when making longitudinal measurements when the zone of injury extends beyond the standard field of view. While a standardized scanning approach to the entire region should always be performed, the athlete’s symptoms should guide a more focused examination in the region of maximal pain. Contralateral examination may be helpful for comparison, particularly in cases of less severe injury. The key components of the ultrasound evaluation of muscle injury include assessment of fluid (hematoma), function (dynamic evaluation of contraction), and flow (increased blood flow/hyperemia on Doppler).
The presence and extent of hematoma should be documented in both short and long axis imaging planes. As mentioned above, 48 h postinjury is likely the ideal time for initial examination. If the examination is performed prior to this time, consider a repeat examination within a few days to document any additional hematoma that may not have been optimally visualized at the initial examination. Posttraumatic hematoma will appear anechoic and will be compressible with transducer pressure (Fig. 2). As healing progresses, the hematoma will begin to organize and may take on a mixed or hyperechoic appearance. If significant hematoma is present, aspiration may be considered. Our current practice is to aspirate any hematoma with estimated volume > 3 to 5 mL.
Functional assessment is typically most useful during follow up scans as presence of initial hematoma implies absence of functional contraction by default. If no hematoma is present on initial examination, then dynamic assessment with isometric contraction is performed. The long axis imaging plane is most helpful when assessing functional contraction across the healing zone of injury. Dynamic examination may help identify regions of more significant fiber disruption if hematoma has not yet developed. Contraction testing also helps identify fascial injury and muscle herniation which should be documented. Short axis imaging is often more helpful with identifying muscle herniation, but multiple imaging planes should be used to take full advantage of this unique capability of ultrasound.
In our experience, resolution of hyperemia on Doppler typically takes the longest and is the final step in the ultrasound component of the return to play progression. As muscle is vascularized tissue, care should be taken to appropriately interpret the presence of true hyperemia within healing scar versus normal blood flow within the muscle. Normal muscle blood flow is typically only appreciated within the hyperechoic fibroadipose septa. The presence of Doppler blood flow within the zone of injury or surrounding a region of scar tissue would be considered abnormal hyperemia. Contralateral comparison or comparison to adjacent noninjured muscle tissue is often helpful in making this distinction. Alterations in the presence or degree of Doppler flow may change in relation to patient activity level prior to the study as well as related to compression or transducer manipulation during the examination (32). Therefore it is recommended that these factors are taken into consideration and standardized during all follow-up examinations.
Interpretation of Ultrasound Findings
The role of the ultrasound evaluation is to complement the functional examination and identify those who appear clinically ready for return to play but may be at high risk of early recurrent injury. After the initial injury grading, the athlete is allowed to progress through the usual rehabilitation protocol for their sport. Once the athlete is able to reach approximately 80% speed/power without symptoms then a repeat ultrasound examination is performed. This number was chosen simply because our experience suggested there is very low risk of recurrent injury when working below 80% speed/power during the rehabilitation phase. Any residual hematoma or lack of functional contraction would be considered high risk for recurrent injury and the athlete likely not allowed to progress. Presence of hyperemia only would be considered intermediate risk, and the athlete may be allowed to continue slow progression with careful monitoring. Repeat ultrasound evaluation is recommended every 1 to 2 wk pending the severity of the remaining abnormal findings (i.e., presence of hematoma vs only minimal hyperemia) as well as competition demands. Ideally, the athlete’s ultrasound evaluation will demonstrate resolution of hematoma and hyperemia and restoration of functional contraction prior to being cleared for full training and/or match selection. The individual demands of the athlete’s sport and position must always be considered.
Another benefit of the serial ultrasound examination is the ability for early identification of myositis ossificans (MO) formation. Although more common in contusive muscle injury, MO can be seen as a complication of strain injuries as well. MO represents ossification of the posttraumatic hematoma (13). The sonographic appearance of MO is characterized by a hyperechoic egg-shell like calcific rim with variable amounts of posterior acoustic shadowing depending on the maturity of the lesion (Fig. 3). MO is identified approximately 2 wk earlier on ultrasound than X-ray (13).
Intramuscular Tendon Involvement
Intramuscular or central tendon injuries have been a topic of recent discussion in the literature. Although still debated, most agree that intramuscular tendon involvement represents a more severe grade of injury and some even advocate for surgical management of a subset of these injuries (4,5,22,33–36). Physical examination alone is not sufficient in identifying intramuscular tendon injury (37). Early detection is paramount, particularly with partial injuries. We have found early return to play and subsequent progression to complete intramuscular tendon disruption leads to significant time loss and in some cases requires surgical management. Following a protocol similar to that outlined above can allow for early identification and close monitoring of these injuries through the return to play process.
Muscle strain injuries will always present a challenge and a multimodal/multidisciplinary approach is needed to reduce risk of reinjury during the return to play process. Serial ultrasound examination can provide valuable real time information regarding the muscle healing process which can complement the traditional functional evaluation. We have found that implementation of the presented protocol has allowed for detection of a subset of athletes whose clinical examination and functional testing suggested they were ready for return to play but whose ultrasound examination demonstrated high-risk features. During formalization of this protocol, several such athletes were allowed to return to play on the basis of clinical criteria and subsequently suffered recurrent injury including progression to intramuscular tendon disruption. We fully acknowledge that a prospective study is needed to validate our approach; however, this protocol is relatively easy to implement and offers insights into muscle healing that have not previously been evaluated.
Disclosures: M.M.H. is a consultant at Tenex Health, Medical Advisor Board Sonex Health.
1. Ekstrand J, Askling C, Magnusson H, et al. Return to play after thigh muscle injury in elite football players: implementation and validation of the Munich muscle injury classification. Br. J. Sports Med
. 2013; 47:769–74.
2. Feeley BT, Kennelly S, Barnes RP, et al. Epidemiology of National Football League training camp injuries from 1998 to 2007
. Am. J. Sports Med
. 2008; 36:1597–603.
3. Mueller-Wohlfahrt HW, Haensel L, Mithoefer K, et al. Terminology and classification of muscle injuries in sport: the Munich consensus statement. Br. J. Sports Med
. 2013; 47:342–50.
4. Patel A, Chakraverty J, Pollock N, et al. British athletics muscle injury classification: a reliability study for a new grading system. Clin. Radiol
. 2015; 70:1414–20.
5. Pollock N, James SL, Lee JC, et al. British athletics muscle injury classification: a new grading system. Br. J. Sports Med
. 2014; 48:1347–51.
6. Dalton SL, Kerr ZY, Dompier TP. Epidemiology of hamstring strains in 25 NCAA sports in the 2009–2010 to 2013–2014 academic years. Am. J. Sports Med
. 2015; 43:2671–9.
7. Eckard TG, Kerr ZY, Padua DA, et al. Epidemiology of quadriceps strains in National Collegiate Athletic Association athletes, 2009–2010 through 2014–2015. J. Athl. Train
. 2017; 52:474–81.
8. van der Horst N, van de Hoef S, Reurink G, et al. Return to play after hamstring injuries: a qualitative systematic review of definitions and criteria. Sports Med
. 2016; 46:899–912.
9. Ekstrand J, Walden M, Hagglund M. Hamstring injuries have increased by 4% annually in men’s professional football, since 2001: a 13-year longitudinal analysis of the UEFA Elite Club injury study. Br. J. Sports Med
. 2016; 50:731–7.
10. Chan O, Del Buono A, Best TM, Maffulli N. Acute muscle strain injuries: a proposed new classification system. Knee Surg. Sports Traumatol. Arthrosc
. 2012; 20:2356–62.
11. Wangensteen A, Del Buono A, Best TM, et al. New MRI muscle classification systems and associations with return to sport after acute hamstring injuries: a prospective study. Eur. Radiol
12. 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; 183:975–84.
13. Peetrons P. Ultrasound of muscles. Eur. Radiol
. 2002; 12:35–43.
14. Takebayashi S, Takasawa H, Banzai Y, et al. Sonographic findings in muscle strain injury: clinical and MR imaging correlation. J. Ultrasound Med
. 1995; 14:899–905.
15. Brassuer J-LR, Mercy G, Gault V, Zeitoun-Ess D. Anatomie echographique et pathologie des ischiojambiers, in actualites en echographie de l’appareil locomoteur. Sauramps Medical
. 2011; 263–308.
16. Fournier-Farley C, Lamontagne M, Gendron P, et al. Determinants of return to play after the nonoperative management of hamstring injuries in athletes: a systematic review. Am. J. Sports Med
. 2016; 44:2166–72.
17. Askling C, Saartok T, Thorstensson A. Type of acute hamstring strain affects flexibility, strength, and time to return to pre-injury level. Br. J. Sports Med
. 2006; 40:40–4.
18. Askling CM, Tengvar M, Saartok T, et al. Acute first-time hamstring strains during slow-speed stretching: clinical, magnetic resonance imaging, and recovery characteristics. Am. J. Sports Med
. 2007; 35:1716–24.
19. De Vos RJ, Reurink G, Goudswaard GJ, et al. Clinical findings just after return to play predict hamstring re-injury, but baseline MRI findings do not. Br. J. Sports Med
. 2014; 48:1377–84.
20. Ekstrand J, Healy JC, Waldén M, et al. Hamstring muscle injuries in professional football: the correlation of MRI findings with return to play. Br. J. Sports Med
. 2012; 46:112–7.
21. Ekstrand J, Lee JC, Healy JC. MRI findings and return to play in football: a prospective analysis of 255 hamstring injuries in the UEFA Elite Club Injury Study. Br. J. Sports Med
. 2016; 50:738–43.
22. Pollock N, Patel A, Chakraverty J, et al. Time to return to full training is delayed and recurrence rate is higher in intratendinous (’c’) acute hamstring injury in elite track and field athletes: clinical application of the British Athletics Muscle Injury Classification. Br. J. Sports Med
. 2016; 50:305–10.
23. Reurink G, Almusa E, Goudswaard GJ, et al. No association between fibrosis on magnetic resonance imaging at return to play and hamstring reinjury risk. Am. J. Sports Med
. 2015; 43:1228–34.
24. Reurink G, Brilman EG, de Vos RJ, et al. Magnetic resonance imaging in acute hamstring injury: can we provide a return to play prognosis? Sports Med
. 2015; 45:133–46.
25. Reurink G, Goudswaard GJ, Tol JL, et al. MRI observations at return to play of clinically recovered hamstring injuries. Br. J. Sports Med
. 2014; 48:1370–6.
26. Reurink G, Whiteley R, Tol JL. Hamstring injuries and predicting return to play: “bye-bye MRI?”. Br. J. Sports Med
. 2015; 49:1162–3.
27. van der Made AD, Almusa E, Whiteley R, et al. Intramuscular tendon involvement on MRI has limited value for predicting time to return to play following acute hamstring injury. Br. J. Sports Med
. 2018; 52:83–8.
28. van Heumen M, Tol JL, de Vos RJ, et al. The prognostic value of MRI in determining reinjury risk following acute hamstring injury: a systematic review. Br. J. Sports Med
. 2017; 51:1355–63.
29. Wangensteen A, Almusa E, Boukarroum S, et al. MRI does not add value over and above patient history and clinical examination in predicting time to return to sport after acute hamstring injuries: a prospective cohort of 180 male athletes. Br. J. Sports Med
. 2015; 49:1579–87.
30. Wangensteen A, Tol JL, Roemer FW, et al. Intra- and interrater reliability of three different MRI grading and classification systems after acute hamstring injuries. Eur. J. Radiol
. 2017; 89:182–90.
31. Wangensteen A, Tol JL, Witvrouw E, et al. Hamstring reinjuries occur at the same location and early after return to sport: a descriptive study of MRI-confirmed reinjuries. Am. J. Sports Med
. 2016; 44:2112–21.
32. Hall MM, Finnoff JT, Sayeed YA, et al. Sonographic evaluation of the plantar heel in asymptomatic endurance runners. J. Ultrasound Med
. 2015; 34:1861–71.
33. Balius R, Maestro A, Pedret C, et al. Central aponeurosis tears of the rectus femoris: practical sonographic prognosis. Br. J. Sports Med
. 2009; 43:818–24.
34. Brukner P, Connell D. Serious thigh muscle strains: beware the intramuscular tendon which plays an important role in difficult hamstring and quadriceps muscle strains. Br. J. Sports Med
. 2016; 50:205–8.
35. Lempainen L, Kosola J, Pruna R, et al. Central tendon injuries of hamstring muscles: case series of operative treatment. Orthop. J. Sports Med
. 2018; 6:2325967118755992.
36. Sonnery-Cottet B, Daggett M, Gardon R, et al. Surgical management of recurrent musculotendinous hamstring injury in professional athletes. Orthop. J. Sports Med
. 2015; 3:2325967115606393.
37. Crema MD, Guermazi A, Reurink G, et al. Can a clinical examination demonstrate intramuscular tendon involvement in acute hamstring injuries? Orthop. J. Sports Med
. 2017; 5:2325967117733434.