Imaging of Muscle Injuries in Sports Medicine: Sports Imaging Series
Abstract
In sports-related muscle injuries, the main goal of the sports medicine physician is to return the athlete to competition—balanced against the need to prevent the injury from worsening or recurring. Prognosis based on the available clinical and imaging information is crucial. Imaging is crucial to confirm and assess the extent of sports-related muscle injuries and may help to guide management, which directly affects the prognosis. This is especially important when the diagnosis or grade of injury is unclear, when recovery is taking longer than expected, and when interventional or surgical management may be necessary. Several imaging techniques are widely available, with ultrasonography and magnetic resonance imaging currently the most frequently applied in sports medicine. This state of the art review will discuss the main imaging modalities for the assessment of sports-related muscle injuries, including advanced imaging techniques, with the focus on the clinical relevance of imaging features of muscle injuries.
© RSNA, 2017
Online supplemental material is available for this article.
An earlier incorrect version of this article appeared online. This article was corrected on September 8, 2017.
Introduction
Muscle injuries represent a major challenge for professional athletes, accounting for up to one-third of all sports-related injuries (1–4), and they are responsible for a large part of time lost to competition (5–8). The main goal of the sports medicine physician is to return the athlete to competition—balanced against the need to prevent the injury from worsening or recurring. Prognosis based on the available clinical and imaging information is crucial. Imaging is crucial to confirm and assess the extent of sports-related muscle injuries and may help to guide management, which directly affects the prognosis. This is especially important when the diagnosis or grade of injury is unclear, when recovery is taking longer than expected, and when interventional or surgical management may be necessary. Several imaging techniques are widely available, with ultrasonography (US) and magnetic resonance (MR) imaging currently the most frequently applied in sports medicine. In this review, we begin with the functional anatomy of the skeletal muscle and the mechanisms of injury. We will discuss the main imaging modalities for the assessment of sports-related muscle injuries, including advanced imaging techniques, with the focus on the clinical relevance of imaging features of muscle injuries. We will also describe the role of imaging in depicting the pathologic finding of overuse of muscles, as well as healing and complications of muscle injuries in athletes.
Mechanisms of Injury and Clinical Features
The most common mechanism of injury of muscles in elite athletes is related to muscle strain (indirect muscle injury), mainly in the lower limbs. Muscles are at risk for disruption during eccentric contraction, as the force of active contraction is added to the passive stretching force applied to the myotendinous junction (MTJ) (9,10). Acute muscle injuries in the lower limbs are associated with both sprinting and stretching activities, mainly affecting the hamstring muscle complex. For these MTJ injuries there is more pronounced loss of function initially but with faster recovery for sprinting-related injuries, while for stretching injuries there is less loss of function initially but slower recovery (7,8,11). Factors related to muscles and activities that increase the risk for indirect muscle injury include eccentric contraction, involvement of muscles with high content of fast twitch type 2 fibers, a sudden change in muscle function, muscles crossing multiple joints (biceps femoris, rectus femoris, gastrocnemius muscles), failure to absorb or counteract forces from other muscle groups or ground reaction, and muscle imbalance (12–14). Indirect mechanisms may further lead to acute avulsion injuries, usually resulting from extreme, unbalanced, and eccentric forces (15). With muscle injuries, athletes present with an immediate sudden onset of pain usually localized in a specific muscle compartment during a period of eccentric contraction, which prevents the athlete from continuing the activity. Flexibility and strength measurements are usually used to obtain additional information on injury severity. Clinically, muscle strains may be categorized into grade 1, no appreciable tissue tearing, with no substantial (less than 5%) loss of function or strength; grade 2, tissue damage of the MTJ with reduced strength and some residual function; and grade 3, complete tear of the myotendinous unit with complete loss of function and occasionally a palpable gap (16).
Blunt trauma is the most common mechanism of direct muscle injury in sports, mainly affecting the lower limbs in sports that may involve collisions as in soccer, football, and rugby. Depending on the dissipation pattern of the blunt force, different degrees of muscle contusion may be observed, usually (but not always) occurring deep in the muscle belly: An intramuscular hematoma may be present. High-grade injury is commonly seen in cases of massive blunt force directed toward the bone, with a massive amount of energy dissipated from the deep muscle to the bone. Penetrating trauma with muscle laceration rarely occurs in elite sports. Clinically, muscle contusions can be categorized as mild (range of motion loss less than one-third with shorter recovery times), moderate (range of motion loss from one-third to two-thirds of normal, with moderate recovery times), and severe contusions (range of motion loss greater than two-thirds with longer recovery times) (9). Muscle contusions tend to show fewer symptoms than muscle strains.
US Assessment of Skeletal Muscle Injuries
Advances in hardware and transducer technology now allow visualization of muscular architecture at in-plane resolution under 200 μm and with a section thickness of 0.5–1.0 mm, which exceeds current MR imaging (17). Although the evaluation of muscle injuries by using MR imaging has been extensively described, US can have a number of distinct advantages: It offers dynamic muscle assessment, it is fast, relatively inexpensive, easier for patients, and allows serial evaluation to follow healing, and it can be used to perform real-time interventions. In addition, US can demonstrate the muscle structure and other relevant anatomy surrounding an injury that can often be obscured by edema on MR images (18).
US Technique
Initial assessment commences with a clinical history and pertinent physical examination. This allows the subsequent US examination to be targeted toward the most relevant areas. The majority of skeletal muscles lie superficially within the body and therefore are optimally assessed by using linear transducers. Modern multifrequency transducers (center frequency greater than 10–17 MHz) allow visualization of most muscle groups. Lower-frequency linear (8–10 MHz) probes may be needed in very muscular patients, especially in the gluteal region and proximal thigh. Modern software and transducers now allow trapezoid fields of view (FOVs) or composite image formation for which the latter can extend the transducer’s FOV to 60 cm. After obtaining the optimal transducer setting, the examination begins with longitudinal and transverse scanning of the symptomatic area. In the majority of muscle injuries, the symptomatic area accurately locates the muscle lesion, but the examiner must be confident of the anatomy being examined and the exact position of the lesion. After assessing the appearance of the muscle and any lesion at rest, the abnormal area and surrounding tissues should be assessed dynamically with active and/or passive contraction. This allows the consistency of the abnormality (eg, solid or cystic), alteration in muscle function, and any movement of disrupted fibers (helping differentiate grades of tears) to become more apparent. Additional maneuvers, especially in the case of muscle hernias, may be required since the hernia may only become apparent when the patient is standing.
US Features
Normal muscle fibers are arranged in parallel hypoechoic bundles (fascicles) surrounded by echogenic fibrofatty septa in a “pennate” configuration (Figs 1 and 2). The muscle fibers and fascicles are of low echogenicity compared with adjacent fascia and nervous tissue. Because of its thickness, the perimysium, which appears relatively echogenic due to its fibrous (collagen) content, can be seen in pennate muscles at longitudinal scanning as multiple parallel lines forming oblique angles (separated by the hypoechoic fascicles) with the MTJ. The orientation of perimysium to the long axis of muscle is oblique in uni-/bipennate muscles and parallel in fusiform muscles. These linear structures converge to the MTJ with the tendon seen as a discrete fibrillar echogenic structure as it becomes more defined. In the transverse plane, the muscle fibers are hypoechoic with the intervening septae seen as smaller linear areas and echogenic “dots.” Finally another thick layer of fascia called the epimysium surrounds the entire muscle and again is echogenic due to its fibrous content.
Figure 1: Transverse sonogram of rectus femoris shows normal echogenic epimysium (white arrowheads), perimysium (arrows) with intervening hypoechoic fascicles, and normal echogenic MTJ (black arrowheads).
Figure 2: Longitudinal extended FOV sonogram of gastrocnemius shows normal echogenic perimysium (arrows) with intervening hypoechoic fascicles converging in a pennate orientation to the MTJ (arrowheads).
The spectrum of US features of muscle strain was previously described by Peetrons (19). In clinically grade 1 injuries, US images may be either negative or exhibit focal or diffuse ill-defined areas of increased echogenicity within the muscle at the site of injury. Grade 1 injuries may also include injuries exhibiting minimal focal fiber disruption occupying less than 5% of the cross-sectional area of the muscle, represented by a well-defined focal hypoechoic or anechoic area within the muscle (Fig 3). There is no consensus about this definition, with some authors considering any degree of partial fiber disruption as a grade 2 injury (9). The presence of areas of partial fiber disruption (less than 100% of the cross-sectional area of the muscle affected) seen at US represents grade 2 injury (Fig 4). Usually, there is discontinuity of the echogenic perimysial striae around either the MTJ or the myofascial junction. An intramuscular hematoma may be depicted as well in grade 2 injuries, and its echogenicity is dependent on the temporal evolution of the injury. Initially (24–48 hours), intramuscular hematomas usually appear as an ill-defined muscle laceration separated by hypoechoic fluid with marked increased reflectivity in the surrounding muscle. During this period, hematomas may solidify and display increased echogenicity in comparison to the surrounding muscle. After 48–72 hours, hematomas will develop into a well-defined hypoechoic fluid collection with an echogenic margin, which gradually enlarges, potentially filling the hematoma in a centripetal fashion (9).
Figure 3: Grade 1 injury of the biceps femoris. Transverse sonogram of left thigh shows normal muscle (*) with a small area of echogenic edematous muscle (arrows) containing a tiny area of hypoechoic disruption (arrowheads).
Figure 4a: Grade 2 injury of the semitendinosus with diffuse leg pain. (a) Transverse and (b) longitudinal sonograms of left thigh show hypoechoic muscle disruption (arrows) with hematoma (arrowheads) also present extending along the disrupted perimysium and abutting the sciatic nerve (*).
Figure 4b: Grade 2 injury of the semitendinosus with diffuse leg pain. (a) Transverse and (b) longitudinal sonograms of left thigh show hypoechoic muscle disruption (arrows) with hematoma (arrowheads) also present extending along the disrupted perimysium and abutting the sciatic nerve (*).
A complete discontinuity or disruption of the MTJ with different degrees of retraction depicted at US represents grade 3 injury (Fig 5). Grade 3 lesions are usually clinically evident with a palpable gap between the retracted ends of the muscle affected. Also, perifascial fluid may be depicted with US, which may have an increased echogenicity due to the presence of extravascular blood but is usually hypoechoic because most examinations occur more than 24 hours after injury. Perifascial fluid detection is not a specific feature as it can occur in any grade of injury.
Figure 5: Grade 3 injury of the medial head gastrocnemius (MHG). Longitudinal extended FOV sonogram shows edematous muscle (medial head gastrocnemius) with complete tear causing retraction (arrowheads) and extensive hematoma (*).
Artifacts and Pitfalls in US Evaluation of Muscle Injury
The linear configuration of the septae makes them susceptible to anisotropy artifact leading to decreased echogenicity or absent of conspicuity of septae, which can be mistaken for an injury. Careful probe repositioning is needed to ensure that the apparent absence of septae is due to the artifact rather than an injury. Other potential sources of artifacts are prominent intramuscular vessels, which can mimic tears. Errors due to this artifact can be avoided through the use of Doppler as well as by carefully tracing of the vessels through the septae to their neurovascular bundles and by determining that the surrounding muscle structure is normal right up to the vessel boundary. Occasionally thickened or scarred septae can cause acoustic shadowing that makes the underlying muscle appear hypoechoic. During exercise, blood flow through the muscle and connective tissues can normally increase 20-fold, with resultant muscle swelling and displacement of the overlying fascial planes (a muscle volume increase of 10%–15%) (17,20).
Routine MR Imaging Assessment of Skeletal Muscle
MR Imaging Technique
MR imaging is considered the reference imaging method to assess the morphology of muscles in athletes owing to its ability to visualize soft tissues with excellent contrast and provide high spatial-resolution and multiplanar assessment, especially in cases in which traumatic lesions are clinically suspected (21,22). MR imaging is well suited to confirm and evaluate the extent and severity of muscle injuries. Furthermore, MR imaging may be better suited than US for the assessment of muscle injuries located in deep muscle compartments. MR imaging is usually performed unilaterally (affected limb only) by using a dedicated surface coil, to ensure higher resolution images with thinner sections and smaller FOV. Simultaneous acquisition of images of the contralateral lower limb by using a higher FOV should be ideally performed in selected cases (eg, when bilateral injury is suspected). The coil selection should be based on the desired FOV. A skin marker (capsule filled with fish oil or vegetable oil) should be placed over the area of symptoms according to the athlete’s orientation, to correlate imaging and clinical features. To accurately evaluate morphology and extent of muscle injuries, multiplanar acquisitions (axial, coronal, and sagittal) are required in regard to the long and short axes of the involved muscle(s). Pulse sequences must include fat-suppressed fluid-sensitive techniques, which allow for the detection of edematous changes around the myotendinous and myofascial junctions, as well as for the delineation of intramuscular or perifascial fluid collections or hematomas. Fluid-sensitive techniques include fat-suppressed (fast or turbo) spin-echo T2-weighted, proton density–weighted, intermediate-weighted sequences, as well as the short tau inversion recovery, or STIR, technique. T1-weighted spin-echo sequences are less sensitive to edematous changes within the muscle in acute injury. However, they may be useful in the assessment of subacute hemorrhage or hematoma, as well as to detect and evaluate the extent of atrophy and fatty infiltration and scar tissue formation in chronic injuries.
MR Imaging Features of Muscle Injury
Most muscle injuries occur around the MTJ. Interstitial edema and hemorrhage around the MTJ may often extend along the adjacent muscle fibers and fascicles, which is detected on fluid-sensitive coronal or sagittal MR images as an ill-defined focal or diffuse high-signal-intensity area along the MTJ seen on images obtained with fluid-sensitive techniques, with a classic feathery appearance (23,24) (Fig 6). The presence of an edematous pattern only, without substantial disruption of muscle fibers or muscle architecture, is commonly referred to as a grade 1 injury (6,25), and loss of muscular function is not usually observed. The tendon at the MTJ usually has normal signal intensity and morphology in a grade 1 injury, with regular contours and marked low signal intensity with all pulse sequences. However, it may also be mildly thickened with abnormal signal intensity, but without disruption or laxity. Mild perifascial fluid may accompany grade 1 injuries. In addition to grade 1 features, the presence of a partial disruption of muscle with hematoma formation around the MTJ is commonly referred to as a grade 2 injury (6,27), with local distortion of muscle architecture. Partial disruption is usually depicted as a focal area of well-defined high signal intensity on images obtained with fluid-sensitive MR imaging sequences (Fig 7). The tendon adjacent to the MTJ may be thickened and exhibit features of laxity, and partial disruption of the tendon may be depicted as well (Fig 8). There is usually some function loss associated with grade 2 injuries on MR images, depending on the extent. Moderate to severe perifascial fluid is often present in grade 2 injuries. Finally, grade 3 injuries on MR images are usually represented by a complete disruption of the MTJ with a local hematoma filling the gap created by the tear (6,27). Clinical examination is usually sufficient to diagnose grade 3 injuries, with complete loss of function, a palpable gap, and muscle retraction observed. Complete avulsion injuries of the MTJ or tendons from the bony attachment are also considered to represent grade 3 injuries (Fig 9). The MR imaging appearance of intramuscular hematomas, which may accompany not only grades 2 and 3 injuries but also muscle contusions (Fig 10), may change according to the predictable pattern of blood degradation, which is not always true for intermuscular (or perifascial) hematomas (9,26). Injuries may occur within the muscle belly and far from the main MTJ, or at the peripheral myofascial junction (around the epimysial interface). One could argue that muscle belly injuries occur from dissipating forces affecting smaller secondary central myoaponeurotic junctions. In injuries at the peripheral myofascial junction, the edema pattern is depicted at the periphery of muscles. These injuries may or may not be associated with focal fascial disruption (Fig 11), as well as with focal partial disruption of the adjacent muscle fibers. Several imaging classification or grading systems for muscle injuries, especially strains, are available for application in clinical practice and clinical research (6,25,27–29). The widely used grading 1–3 system (6) for muscle injuries, as discussed above, lacks diagnostic accuracy and provides limited prognostic information to sports medicine physicians, since it does not properly cover the full spectrum of muscle injury features. Potentially clinically relevant imaging features should be included in a grading system, which should be capable of providing prognostic information and a diagnostic framework for enhanced clinical decision making in the management of muscle injuries. A consensus statement on new terminology and classification of muscle injuries in sports was published in 2013 (27), which defined grades based on the cause of injuries. The “functional” classes are grade 1 for fatigue-induced disorders and delayed-onset muscle soreness (DOMS); spine-related and muscle-related neuromuscular disorders are grade 2 injuries. The “structural” classes refer to an indirect injury mechanism and include partial muscle tears as grade 3 and subtotal/complete discontinuity of muscle/tendon as grade 4 injuries (Table). Direct injuries leading to muscle contusion or laceration are considered separately in such consensus.
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Figure 6a: (a) Coronal and (b) axial proton-density fat-suppressed MR images of the thigh (a, repetition time msec/echo time msec, 3900/25; FOV, 23 × 33 cm; section thickness, 4 mm; intersection gap, 1 mm; b, 3900/24; FOV, 28 × 28 cm; section thickness, 5 mm; intersection gap, 1.2 mm). MR grade 1 injury of the semimembranosus muscle is seen, exhibiting the classic feathery pattern of ill-defined muscle edema on the coronal image (a). Note the edema is mainly distributed around the MTJ, with the central tendon exhibiting normal low signal intensity and thickness (arrows). Note mild perifascial fluid.
Figure 6b: (a) Coronal and (b) axial proton-density fat-suppressed MR images of the thigh (a, repetition time msec/echo time msec, 3900/25; FOV, 23 × 33 cm; section thickness, 4 mm; intersection gap, 1 mm; b, 3900/24; FOV, 28 × 28 cm; section thickness, 5 mm; intersection gap, 1.2 mm). MR grade 1 injury of the semimembranosus muscle is seen, exhibiting the classic feathery pattern of ill-defined muscle edema on the coronal image (a). Note the edema is mainly distributed around the MTJ, with the central tendon exhibiting normal low signal intensity and thickness (arrows). Note mild perifascial fluid.
Figure 7: Axial proton-density fat-suppressed MR image of the thigh (3900/24; FOV, 28 × 28 cm; section thickness, 5 mm; intersection gap, 1.2 mm). MR grade 2 injury of the semimembranosus muscle, with a focal partial tear (fiber disruption) represented by a fairly well-defined area of high signal intensity (arrows) adjacent to the MTJ (tendon demonstrated by arrowheads). Note mild perifascial fluid.
Figure 8a: (a) Axial and (b) coronal proton-density fat-suppressed MR images of the thigh (a, 3900/24; FOV, 28 × 28 cm; section thickness, 5 mm; intersection gap, 1.2 mm; b, 3900/25; FOV, 23 × 33 cm; section thickness, 4 mm; intersection gap, 1 mm). Marked thickening and signal intensity changes of the central tendon at the proximal MTJ of the long head of biceps femoris muscle (arrows), with blurring of the tendon contours and foci of partial discontinuity, mainly observed in b (arrows). Discontinuity of the central tendon at the MTJ of the long head of biceps femoris seen with MR imaging was shown to be associated with longer recovery times in athletes (Reurink et al, 73). Note mild perifascial fluid.
Figure 8b: (a) Axial and (b) coronal proton-density fat-suppressed MR images of the thigh (a, 3900/24; FOV, 28 × 28 cm; section thickness, 5 mm; intersection gap, 1.2 mm; b, 3900/25; FOV, 23 × 33 cm; section thickness, 4 mm; intersection gap, 1 mm). Marked thickening and signal intensity changes of the central tendon at the proximal MTJ of the long head of biceps femoris muscle (arrows), with blurring of the tendon contours and foci of partial discontinuity, mainly observed in b (arrows). Discontinuity of the central tendon at the MTJ of the long head of biceps femoris seen with MR imaging was shown to be associated with longer recovery times in athletes (Reurink et al, 73). Note mild perifascial fluid.
Figure 9a: (a) Axial and (b) coronal proton-density fat-suppressed MR images of the thigh. A complete avulsion of the proximal hamstring tendons (grade 3 injury) is depicted at the ischial tuberosity (arrows, a). Note the adjacent sacrotuberous ligament (arrowheads). There is marked distal retraction of the proximal MTJs (arrows, b), with a voluminous hematoma filling the gap (*).
Figure 9b: (a) Axial and (b) coronal proton-density fat-suppressed MR images of the thigh. A complete avulsion of the proximal hamstring tendons (grade 3 injury) is depicted at the ischial tuberosity (arrows, a). Note the adjacent sacrotuberous ligament (arrowheads). There is marked distal retraction of the proximal MTJs (arrows, b), with a voluminous hematoma filling the gap (*).
Figure 10: Axial proton-density fat-suppressed image (3900/24; FOV, 28 × 28 cm; section thickness, 5 mm; intersection gap, 1.2 mm) shows an intramuscular hematoma at the semitendinosus muscle after direct trauma (arrows), represented by a well-defined collection with a thick wall and heterogeneous content, with a fluid-fluid level. Note moderate perifascial fluid.
Figure 11: Coronal proton-density fat-suppressed MR image of the thigh (3900/25; FOV, 23 × 33 cm; section thickness, 4 mm; intersection gap, 1 mm) demonstrates injury of the long head of biceps femoris muscle affecting the myofascial junction, with a focal complete tear (disruption) of the adjacent fascia (arrows).
Advanced MR Imaging Techniques
To date, the main advanced MR imaging techniques available for muscle assessment are not applied routinely in clinical practice. These techniques are mainly explored in clinical research and have a great potential to be applied in a sports medicine setting. T2 mapping may be useful from a sports medicine perspective. As T2 values increase in stressed muscles, it is possible to isolate the activated muscles after specific exercises (30) (Fig 12). In some cases even the degree of activation (including muscle activity and muscle strength) can be assessed, as these may be related to the degree of increase in T2 values (30,31). Diffusion tensor imaging allows diffusion quantification of anisotropic tissues (eg, muscle) using a series of diffusion-weighted images and subsequent muscle fiber tracking. Diffusion tensor imaging has been shown to be useful for tracking skeletal muscle fiber direction, detecting subclinical changes in muscles after strenuous exercise, detecting muscle injury on a microscopic level, and differentiating injured muscles from normal control muscles (32–34). Skeletal muscle MR elastography can be used for studying the physiologic response of normal (Fig 13) or diseased and damaged muscles. In fact, it has been found that there is a difference in the stiffness of muscles with and without neuromuscular disease (35,36).
Figure 12a: T2 mapping of the right leg of a 31-year-old male volunteer (a) before and (b) 3 minutes after plantar flexion exercise. Parameters of the 3.0-T fat-saturated two-dimensional multi–spin-echo sequence were as follows: matrix size, 128 × 102; FOV, 160 × 130 mm; section thickness, 3 mm; repetition time, 3000 msec; echo times, 10–130 msec (number of echoes = 13); bandwidth, 300 Hz/pixel; refocusing angle, 180°; scan time, 5:15 minutes. Note an increase in T2 values in the gastrocnemius muscles after exercise (arrows) when compared with a.
Figure 12b: T2 mapping of the right leg of a 31-year-old male volunteer (a) before and (b) 3 minutes after plantar flexion exercise. Parameters of the 3.0-T fat-saturated two-dimensional multi–spin-echo sequence were as follows: matrix size, 128 × 102; FOV, 160 × 130 mm; section thickness, 3 mm; repetition time, 3000 msec; echo times, 10–130 msec (number of echoes = 13); bandwidth, 300 Hz/pixel; refocusing angle, 180°; scan time, 5:15 minutes. Note an increase in T2 values in the gastrocnemius muscles after exercise (arrows) when compared with a.
Figure 13a: Demonstration of exercise-induced muscle alterations on MR elastograms produced from multifrequency MR elastography data, in a 28-year-old male volunteer. Data were acquired (a) before and (b) 48 hours after an eccentric exercise protocol consisting of 12 sets of eccentric contractions performed on a dynamometer. Increased magnitude shear stiffness is evident on the postexercise elastogram in the rectus femoris and vastus intermedius muscle groups (arrows) when compared with pre-exercise elastogram. Use the color map to compare shear stiffness values between a and b. (Images courtesy of Paul Kennedy, University of Edinburgh, Scotland.) (MR elastography parameters: 1600/54, section thickness, 2 mm; bandwidth, 1560 Hz/pixel; matrix, 112 × 112; FOV, 224 × 224 mm; resolution; 2 mm isotropic; five sections, two signals acquired, eight phase offsets, one motion encoding gradient cycle at 50 Hz, motion encoding in phase-encoding, section-select, and readout direction. Frequencies acquired = 25, 37.5, 50, and 62.5 Hz.)
Figure 13b: Demonstration of exercise-induced muscle alterations on MR elastograms produced from multifrequency MR elastography data, in a 28-year-old male volunteer. Data were acquired (a) before and (b) 48 hours after an eccentric exercise protocol consisting of 12 sets of eccentric contractions performed on a dynamometer. Increased magnitude shear stiffness is evident on the postexercise elastogram in the rectus femoris and vastus intermedius muscle groups (arrows) when compared with pre-exercise elastogram. Use the color map to compare shear stiffness values between a and b. (Images courtesy of Paul Kennedy, University of Edinburgh, Scotland.) (MR elastography parameters: 1600/54, section thickness, 2 mm; bandwidth, 1560 Hz/pixel; matrix, 112 × 112; FOV, 224 × 224 mm; resolution; 2 mm isotropic; five sections, two signals acquired, eight phase offsets, one motion encoding gradient cycle at 50 Hz, motion encoding in phase-encoding, section-select, and readout direction. Frequencies acquired = 25, 37.5, 50, and 62.5 Hz.)
Overuse Muscle Injuries in Sports
In addition to muscle strain, other muscle pathologies related to different sports activities may result in pain and disability. Different from muscle strains, DOMS is an overuse injury related to physical activity, with muscle pain developing hours to days after a specific activity. A decrease of muscle function and strength can be observed. It has been demonstrated that eccentric muscle activity plays a major role in precipitating DOMS (37–42). Pain associated with DOMS typically reaches a peak from 24 to 72 hours after physical activity, then decreases slowly. Such clinical presentation is different from muscle strains, with their immediate onset of pain, and represents the main key to diagnosis. The imaging features of DOMS may be similar to muscle strain, making it sometimes difficult to differentiate these two entities based on imaging features alone. Muscle edema is depicted as high signal intensity of the affected muscle belly at fluid-sensitive MR imaging sequences, and perifascial fluid may be present at the early phase of injury. There is no macroscopic fiber disruption or tear associated with DOMS. However, in some cases, DOMS may present with diffuse edema involving the affected muscle belly, not exhibiting the typical “feathery” pattern of strains and without perifascial fluid (Fig 14). There is no linear relationship between the signal intensity on T2-weighted images and clinical symptoms, with a delay between the occurrence of severe symptoms and the maximum intensity of signal abnormalities seen on MR images (43,44). The resolution of symptoms and re-establishment of muscle function occur within a period of 10–12 days, whereas abnormal signal intensity on fluid-sensitive MR images may last up to 80 days (44).
Figure 14: DOMS. Sagittal proton-density fat-suppressed image (3670/25; FOV, 26 × 33 cm; section thickness, 4 mm; intersection gap, 1 mm) shows diffuse edema of the semitendinosus muscle (arrows) in this soccer player complaining of pain that developed 36 hours after intense training. The classic feathery pattern of strain is not observed in this case, and no fiber disruption is depicted. There is no associated perifascial fluid.
Chronic exertional compartment syndrome (CECS) is typically observed in young athletic individuals and is characterized by chronic and recurrent pain induced by physical activity, mainly due to abnormal increase of tissue pressures that lead to reduced perfusion and ischemic pain (45–48). The pathophysiology of elevated tissue pressures is not fully understood. Several muscle compartments of the lower and upper limbs may be affected, with—in decreasing frequency—the anterior, deep posterior, lateral, and superficial posterior muscle compartments of the lower limbs the most commonly involved (49). The typical clinical manifestation of CECS refers to onset of pain in a specific muscle compartment after initiation of a specific physical activity, with increasing pain intensity with continued activity. Pain usually decreases and resolves with rest. Diffuse tenderness over the affected compartment may be documented during clinical examination only after exercise and provocation of symptoms. The reference standard for the diagnosis of CECS is intracompartmental pressure monitoring, with pressures recorded both before and immediately after exercise. This is done by introducing a needle into the affected compartment and monitoring the pressure with a transducer. Postactivity (postexertional) MR imaging may help in the diagnosis of CECS as, unlike asymptomatic subjects, there is usually a greater and mostly delayed increase in T2 signal intensity of the affected compartment after exercise (50). Subjects not affected by CECS exhibit peak muscle T2 signal intensity during exercise (50), which tends to normalize 15 minutes after exercise. In contrast, in subjects with CECS the T2 signal peaks in the first recovery phase after exercise, with persistence of abnormal T2 signal intensity after several minutes. A change in T2 values in muscles (before and after exertion) of more than 20% has been suggested as positive for CECS. The specific exercise to be applied in patients or athletes in the radiology facility is often the same one that is responsible for the onset of pain while training or competing, and in most cases it can be accomplished within the facility (ideally the exercise is stopped when pain is produced). Advanced MR imaging techniques such as diffusion tensor imaging also show promise in the evaluation of CECS (51). As in compartmental syndromes, the increase in compartmental pressure may lead to decreased muscle vascular flow which may be depicted with contrast-enhanced imaging techniques (Fig 15) and which can lead to myonecrosis.
Figure 15a: Compartment syndrome affecting the extensor and anterior compartments of the right leg. (a) Axial T2-weighted fat-suppressed MR image (3900/52; FOV, 20 × 20 cm; section thickness, 5 mm; intersection gap, 1.0 mm). (b) T1-weighted fat-suppressed MR image after intravenous gadolinium-based contrast agent injection (824/18; FOV, 20 × 20 cm; section thickness, 5 mm; intersection gap, 1.0 mm). Note the extensive muscle edema (arrows, a) and the extensive lack of enhancement after intravenous contrast agent injection (arrows, b), indicating compromised blood supply.
Figure 15b: Compartment syndrome affecting the extensor and anterior compartments of the right leg. (a) Axial T2-weighted fat-suppressed MR image (3900/52; FOV, 20 × 20 cm; section thickness, 5 mm; intersection gap, 1.0 mm). (b) T1-weighted fat-suppressed MR image after intravenous gadolinium-based contrast agent injection (824/18; FOV, 20 × 20 cm; section thickness, 5 mm; intersection gap, 1.0 mm). Note the extensive muscle edema (arrows, a) and the extensive lack of enhancement after intravenous contrast agent injection (arrows, b), indicating compromised blood supply.
Healing and Complication of Muscle Injuries
Pathophysiology of Muscle Healing
In most types of muscle injuries the repair and healing mechanisms are commonly characterized by three stages (52). The initial destruction and inflammatory phase, which usually starts immediately after injury, is characterized by rupture and ensuing necrosis of muscle fibers and the formation of hematoma. Since days 2 and 3, the repair phase initiates at the site of injury, consisting of phagocytosis of necrotic tissue, concomitant production of a connective tissue scar accompanied by capillary ingrowth at the injury site, and activation of satellite cells in the regeneration that will differentiate into myoblasts, ultimately responsible of regeneration of the skeletal muscle. Last is the remodeling phase during which maturation of the regenerated fibers, reorganization of scar tissue, and recovery of the functional capacity of the muscle occur. The latter two phases—repair and remodeling—tend to overlap (53), and their duration depends on the injuries’ initial extent. Hemorrhage allows inflammatory cells such as neutrophils and macrophages to enter the site of injury, and an inflammatory response associated with edema at and surrounding the injury site is observed shortly after injury (54).
Once the destruction phase has subsided, the actual repair of the injured muscle occurs concomitantly with regeneration of disrupted fibers and formation of a connective tissue scar. During phagocytosis, the basal lamina is left intact by macrophages, which acts as scaffolding for reconstitution of the myofibril. Undifferentiated reserve cells called satellite cells below the basal lamina of each individual fiber proliferate, differentiate into myoblasts, fuse to form multinucleated myotubes, and then unite with the remaining portion of injured myofibers (52). Key events during the remodeling phase include contraction and reorganization of scar tissue, maturation of regenerated myofibrils, gradual resolution of edema, and revascularization of the injured portion of muscle (53).
Healing and Postinjury Assessment at MR Imaging
While muscle injuries heal there is a decrease in fluidlike signal intensity at the site of injury on MR images (18). Scar tissue has been observed as early as 6 weeks after initial injury, which can display low signal intensity on T1-weighted and high signal intensity on fluid-sensitive MR images at early stages. At late stages, scar tissue usually displays low signal intensity for all MR imaging pulse sequences. Residual scarring can cause misdiagnosis, leading to both over- and underidentification of new injuries (55). In the weeks to months after injury during the healing phase, differences in the hydrogen and proton environment due to obtained structural tissue changes including (micro) hemorrhage may contribute to susceptibility artifacts that may be observed during follow-up (56). Silder and colleagues evaluated MR imaging morphologic changes of musculotendon remodeling following a hamstring strain injury by using quantification of the muscle-tendon scar volumes. They reported that two-thirds of previously injured subjects had residual scarring at the presumed injury site and concluded that the long-term changes in musculotendon structure following injury alter the mechanics of contraction during movement and may raise the risk of reinjury (57). A recent study found that MR imaging changes may be observed after clinical resolution of symptoms, with 89% of recovered hamstring injuries showing some degree of intramuscular increased signal intensity on fluid-sensitive sequence images (Figs 16, 17). At return to play, one-third of clinically recovered hamstring injuries show low signal intensity suggestive of newly developed fibrous tissues on MR images. The clinical relevance of this finding and its possible association with increased risk of reinjury is uncertain (58).
Figure 16: MR findings of chronic muscle injury. Axial T2-weighted fat-suppressed image (640/21; FOV, 350 × 350 mm; 6 mm section thickness with no intersection gap) of the upper thigh of a 23-year-old male soccer player shows diffuse low-grade hyperintensity signal intensity changes in the adductor longus muscle (arrowheads). The signal intensity alterations are subtle and may persist markedly beyond full clinical recovery. Acute grade 1 lesions are commonly more focal involving only specific parts of a given muscle. Note circumscribed hypointensity medially consistent with beginning fibrosis (arrow).
Figure 17: MR imaging findings of chronic muscle injury. Remote injury to the psoas muscle in a 29-year-old male handball player occurred 6 months prior. Axial intermediate-weighted fat-suppressed image (692/23; FOV, 350 × 350 mm; 6 mm section thickness, no intersection gap) of the pelvis shows subtle residual hyperintensity signal intensity changes surrounding the central tendon (arrows). The player had returned to competition 3 months prior and was symptom-free in regard to this lesion at the time of imaging.
Healing and Postinjury Assessment at US
US findings observed during normal healing depend on the nature of the original injury and initial sonographic findings. Minor or grade 1 injuries may appear with increased echogenicity during healing on US studies, which has been documented in up to 50% of cases of grade 1 injuries (59). In this situation, normal healing is considered a reduction in size or resolution of the region of increased echogenicity. More substantial (grade 2) injuries may present as hypoechoic regions indicative of fluid adjacent muscle fibrils or adjacent to the epimysium (19). Resolution or substantial decrease in the quantity of fluid is to be expected during the normal healing process. Any hematoma or fluid collection should decrease in size, and macroscopic muscle tears may demonstrate echogenicity of the margins of the tear as healing occurs. Over time small tears may fill with echogenic material, likely representing scar tissue. US is less sensitive than MR imaging to residual morphologic changes after muscle injury, because of the higher soft-tissue contrast and high sensitivity to extracellular fluid offered by MR imaging (60). Demonstration of scar tissue during follow-up is of significance because it is likely that more extensive scarring results in increased likelihood of recurrent injury (21). A scar is biomechanically stronger than the native muscle-tendon unit, and it is important to identify these areas of scarring because recurrent injuries may occur nearby (21). The major advantage of US for the evaluation of healing in muscle injuries is the ability to perform dynamic assessment before and after muscle contraction, which may or may not depict persistence of fiber disruption after clinical management and rehabilitation (Movies 1 and 2 [online]).
To date, there is no strong evidence in the literature that imaging follow-up should be routinely performed in athletes sustaining muscle injuries, nor this would relevantly affect management and prognosis. Based on both literature data and clinical experience, we find that follow-up imaging may be useful in two situations: one, for grade 2 injuries (partial fiber disruption) for which clinical symptoms persist after proper management and rehabilitation, being ideally assessed with dynamic US before and after muscle concentric contraction (see Movie 1 (online); and two, in cases of clinical suspicion of reinjury, a follow-up US or MR imaging examination may be performed to reassess these injuries. Reinjuries usually display the same imaging features of acute injuries but may occur in a different location within the same muscle or within another muscle of the same muscle group.
Movie 1. An initial grade 2 strain of the long head of biceps femoris muscle 6 weeks after treatment and rehabilitation. Although static US examination exhibited features suggestive of scar tissue, at dynamic US during concentric contraction of the muscle we can still see the gap, indicating that the healing process is not complete.
Movie 2. An initial grade 2 strain of the long head of biceps femoris muscle 8 weeks after treatment and rehabilitation. There is no gap depicted around the scar tissue during dynamic US with concentric contraction of muscle.
Complications of Muscle Injuries
Muscle hernias.—Muscle hernias are a rare complication and are a result of direct trauma to a muscle, which may herniate through a small fascial defect. The lower extremities are most commonly involved, with the tibialis anterior the most frequently affected (61). Clinically, these patients may present with a chronic mass with or without exertional pain. Imaging is typically not required except where there is clinical uncertainty or the patient needs reassurance. Imaging may not identify any abnormality if there is no herniation at the time of the examination. For this reason US or dynamic MR imaging should be performed also. On US images, normal muscle tissue may be seen extending through a focal fascial defect (Fig 18) (55). The hernia may become more pronounced with contraction. If no abnormality is found, standing with flexion and extension may demonstrate the defect more effectively. Often it is best to ask the patient what produces their lump or what typically produces their pain. On MR images often a subtle contour deformity can be identified with associated edema or a focal outpouching of the muscle through the fascial defect (62).
Figure 18: Muscle hernia of extensor digitorum longus. Transverse extended FOV sonogram shows extensor digitorum longus (EDL) with epimyseal defect (arrows) and muscle hernia (arrowheads). A thick layer of coupling gel (*) has been applied so probe pressure does not reduce the hernia.
Myositis ossificans traumatica.—Posttraumatic myositis ossificans (PTMO) is a nonneoplastic proliferation of bone and cartilage within the skeletal muscle at the site of previous trauma or repeated injury and/or hematoma (63). Being a rare complication, there is little evidence regarding the pathogenesis or the optimal treatment. PTMO most commonly affects the thigh and arm, with anterior muscle groups affected more frequently than the posterior groups (64). Proximal regions of an extremity are more frequently affected than distal parts (65). In sports, myositis ossificans is typically associated with prior sports-related muscle injury, the incidence being highest in the contact sports in which the use of protective devices is uncommon, such as rugby (66). Although it is sometimes possible to detect the first signs of ectopic bone on radiographs as early as 18–21 days after the injury, the formation of ectopic bone usually lags behind the symptoms by weeks, and thus, a definite radiographic diagnosis can only be made substantially later (67). Although PTMO is a benign self-limiting condition, imaging is an important tool to exclude infection or malignancy. Imaging plays an important role especially in the acute stages, when biopsy or excision should be avoided.
PTMO has a characteristic peripheral calcification pattern, not typically seen in other calcifying soft-tissue lesions (Fig 19) (68). Increased vascularity may be depicted on at Doppler US assessment. US may further help in detecting associated calcifications not visualized on radiographs.
Figure 19a: PTMO in a 22-year-old woman who noted, incidentally, a solid mass at the anterior right thigh that was movable beneath the surface. There was previous history of minor direct contact trauma during a hockey game 9 months earlier. (a) Axial nonenhanced computed tomography (CT ) image shows a peripherally calcified lesion (arrows) in the rectus femoris muscle (5-mm reconstructed section thickness). (b) On axial T1-weighted nonenhanced MR image (612/18; FOV, 250 × 250 mm; 5 mm section thickness; 1 mm intersection gap), the lesion (arrows) appears hypointense to muscle. No areas of hyperintensity are seen that would reflect lipomatous or hemorrhagic components. (c) Coronal T1-weighted MR image obtained after contrast agent administration (632/24; FOV, 350 × 350 mm; 5 mm section thickness; 1 mm intersection gap) shows marked inhomogeneous enhancement of the lesion (arrows). Note the peripheral disposition of the calcifications is better depicted with CT than MR imaging.
Figure 19b: PTMO in a 22-year-old woman who noted, incidentally, a solid mass at the anterior right thigh that was movable beneath the surface. There was previous history of minor direct contact trauma during a hockey game 9 months earlier. (a) Axial nonenhanced computed tomography (CT ) image shows a peripherally calcified lesion (arrows) in the rectus femoris muscle (5-mm reconstructed section thickness). (b) On axial T1-weighted nonenhanced MR image (612/18; FOV, 250 × 250 mm; 5 mm section thickness; 1 mm intersection gap), the lesion (arrows) appears hypointense to muscle. No areas of hyperintensity are seen that would reflect lipomatous or hemorrhagic components. (c) Coronal T1-weighted MR image obtained after contrast agent administration (632/24; FOV, 350 × 350 mm; 5 mm section thickness; 1 mm intersection gap) shows marked inhomogeneous enhancement of the lesion (arrows). Note the peripheral disposition of the calcifications is better depicted with CT than MR imaging.
Figure 19c: PTMO in a 22-year-old woman who noted, incidentally, a solid mass at the anterior right thigh that was movable beneath the surface. There was previous history of minor direct contact trauma during a hockey game 9 months earlier. (a) Axial nonenhanced computed tomography (CT ) image shows a peripherally calcified lesion (arrows) in the rectus femoris muscle (5-mm reconstructed section thickness). (b) On axial T1-weighted nonenhanced MR image (612/18; FOV, 250 × 250 mm; 5 mm section thickness; 1 mm intersection gap), the lesion (arrows) appears hypointense to muscle. No areas of hyperintensity are seen that would reflect lipomatous or hemorrhagic components. (c) Coronal T1-weighted MR image obtained after contrast agent administration (632/24; FOV, 350 × 350 mm; 5 mm section thickness; 1 mm intersection gap) shows marked inhomogeneous enhancement of the lesion (arrows). Note the peripheral disposition of the calcifications is better depicted with CT than MR imaging.
Clinical Relevance of Imaging Findings
Return to Play Prediction
In the elite-athlete setting, MR imaging is considered by some as the modality of choice for predicting time to return to sport after acute muscle injury. Current literature on return to play determination is limited to hamstring-related research applying MR imaging as the imaging modality, since assessment of return to play remains one of the major challenges in dealing with acute hamstring injuries. Previous research has suggested that a number of imaging findings are associated with the time needed to return to play (6,7,11,18,69–72).
However, a recent systematic review found that currently there is no strong evidence that any 1.5-T MR imaging finding is useful for predicting the time to return to sports following hamstring injury (73). This conclusion was predominantly based on the considerable risk of bias in most studies and the wide variation in time to return, independent of injury severity. The major methodological flaw of the reviewed studies was a lack of blinding of the subjects and clinicians to the MR imaging findings and simple univariate statistical analysis. Also it must be remembered that it is difficult to apply a standard imaging finding to all athletes when they vary greatly in the muscle range and function required to perform specific activities in different sports, which is reflected in the heterogeneity of muscle injuries. Differences and variations in MR imaging protocols used for hamstring injury research are substantial, suggesting that there is no widely accepted reference standard.
Despite these limitations, the review reported limited to moderate evidence for an association of high signal intensity on T2-weighted images affecting the proximal or central tendon, injuries not affecting the MTJ, and complete ruptures with a longer period to return (73).
Recent studies with a more robust design and using multivariate statistical analysis confirmed that the value of 1.5-T MR imaging or US for predicting return to play was negligible and added little to patient history and clinical examination (74,75). Based on the recent literature, routine MR imaging examination therefore cannot be recommended to provide accurate information for prediction of time to return to play after acute hamstring injuries. Nonetheless, this does not imply that MR imaging should be abandoned from daily practice, as it might be of value for confirming the clinical diagnosis, informing the athlete (the images might give the athlete more understanding of the injury), and living up to the expectation of performing imaging in the elite-athlete setting (76).
Imaging at Return to Play
It is a major challenge to decide whether an athlete can safely return to play, as there are no validated criteria to guide the decision. In clinical practice, MR imaging has been suggested to assist return-to-play decisions (77). Only three studies have been published and all focused on MR imaging at return to play following hamstring injury. These studies showed persisting increased signal intensity on fluid-sensitive images at return to sport clearance (57,78,79). Normalization of increased signal intensities on MR images is therefore not required for a successful return to play, suggesting that functional recovery precedes structural recovery at imaging.
Risk of Reinjury
High reinjury rates remain a major problem following acute muscle injuries. Reinjuries are often more severe than the initial injury and are associated with a longer absence from sports. Studies have focused on the association of MR imaging parameters and reinjury risk. Especially in hamstring injuries, this association has been studied at two clinically relevant time points: at injury and at return to play. At injury, conflicting results on the predictive value of the MR imaging findings for reinjury have been reported. Studies in Australian rules football revealed only limited evidence that the extent of high-signal-intensity changes seen on T2-weighted images (representing the edemalike changes in muscle injuries), measured by using the longitudinal length and the cross-sectional area, is related to an increased risk of reinjury (69,80). Such relationship was not confirmed in a cohort of European professional soccer players (81), Australian rules footballers (71), and amateur soccer players (82). Confirmation of a clinically suspected biceps femoris long head injury with MR imaging might guide the clinician in predicting the reinjury risk, as the reinjury risk is 16% compared with 2% for the medial injured group (81).
An MR imaging examination at return to play cannot be used to predict which athletes will reinjure and which will not, which is a reflection of the heterogeneity of sports-related muscle injuries. At return to play, persisting T2 high-signal-intensity changes will be present in the majority of cases (58,79,83), and these changes are not associated with an increased reinjury risk. At return to play, an area of abnormal intramuscular low signal intensity on T1-weighted images, suggestive for fibrosis, can be expected in approximately one-fourth of the athletes. These low-signal-intensity abnormalities, however, do not seem to be associated with an increased risk of reinjury (78).
In summary, with our current 1.5-T protocols, there is no evidence to support the use of MR imaging for identifying athletes at increased risk of reinjury following acute hamstring injury.
No evidence of clinical relevance regarding prognostication and management exists in the literature for all other imaging features described previously in this review but not mentioned in this section.
Summary
Competitive athletes are at a high risk for acute and repetitive muscle injury, mainly in the lower limbs. Although the clinical examination remains the core of any patient assessment, radiology plays an increasingly important role in the initial assessment and follow-up of muscle injury. The most common mechanism leading to injury of muscles in elite athletes is indirect trauma. Such acute muscle injuries in the lower limbs are associated with both sprinting and stretching activities, mainly affecting the hamstring muscle complex. Blunt trauma is the most common mechanism of direct muscle injury in sports, also primarily affecting the lower limbs, and commonly a result of collisions as seen in soccer, football, and rugby. Muscle injuries are responsible for a large proportion of time lost to competition, and for all professional but also high-level amateur athletes rapid return to training and competition is a priority while minimizing the risk for of recurrent injury.
Appropriate management decisions, return to training and competition, and prediction of injury recurrence may all be influenced by appropriate imaging. Because of the ability to visualize soft tissues with excellent contrast, high-spatial-resolution, and multiplanar assessment, MR imaging seems to be the current imaging method of choice for the initial diagnosis and follow-up of acute muscle injuries, including grade 1 (low-grade damage reflected as diffuse intramuscular hyperintensity) to grade 3 (complete muscle disruption) intramuscular injuries, direct contusions, and musculotendinous avulsion injuries. US may play an important role as an adjunct imaging method. It offers dynamic muscle assessment, is fast and relatively inexpensive, and allows serial evaluation of the healing process. During follow-up of muscle injury, imaging may be particularly helpful in the longitudinal assessment of grade 2 injuries exhibiting partial muscle fiber disruption whenever clinical symptoms persist after proper management and rehabilitation, as well as in cases of a clinical suspicion of reinjury.
Many sports medicine physicians have learned to appreciate high-quality imaging to help guide athlete rehabilitation, although the clinical evaluation itself must guide the final return-to-play decision.
Essentials
■ US offers dynamic muscle assessment and is fast, relatively inexpensive, and easier for patients, allowing for detection and severity assessment of muscle injuries in athletes, as well as for serial evaluation to follow healing; it can be used to guide real-time interventions.
■ The major advantage of US for the evaluation of healing in muscle injuries is the ability to perform dynamic assessment before and after muscle contraction, which may depict persistence of fiber disruption after clinical management and rehabilitation.
■ MR imaging is considered the reference imaging method to assess the morphology of muscles in athletes and is well suited to confirm and evaluate the extent and severity of muscle injuries in athletes through MR imaging–based classification systems.
■ There is sparse evidence that MR imaging–depicted injuries affecting the proximal or intramuscular tendon, injuries not affecting the myotendinous junction, and complete ruptures are associated with a longer period to return to training or competition.
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Article History
Received February 10, 2016; revision requested April 8; revision received September 13; accepted October 10; final version accepted December 14.Published online: Feb 20 2017
Published in print: Mar 2017
