Skeletal Radiol (2014) 43:805–812 DOI 10.1007/s00256-014-1856-z

SCIENTIFIC ARTICLE

Soleus muscle injury: sensitivity of ultrasound patterns Ramon Balius & Gil Rodas & Carles Pedret & Lluís Capdevila & Xavier Alomar & David A. Bong

Received: 19 November 2013 / Revised: 7 February 2014 / Accepted: 21 February 2014 / Published online: 14 March 2014 # ISS 2014

Abstract Objective To assess the sensitivity of ultrasound in detecting soleus muscle lesions diagnosed on magnetic resonance imaging (MRI) and to characterize their location, ultrasound pattern, and evolution. Materials and methods Ultrasound and MRI studies were performed between May 2009 and February 2013 on all patients who presented to the Medical Services Clinic of the Catalan Sport Council with the initial onset of sharp pain in the calf compatible with injury of the soleus muscle. An interobserver ultrasound reliability study was also performed. Results A total of 55 cases of soleus injury were studied prospectively (22 with right leg involvement, 33 left) by ultrasound and MRI, which was utilized as the “gold R. Balius Sport Catalan Council, Generalitat de Catalunya, Barcelona, Spain R. Balius : C. Pedret Clínica CMI Diagonal, Barcelona, Spain G. Rodas F.C. Barcelona Medical Services, Barcelona, Spain C. Pedret (*) Sports Medicine and Imaging Department, Clínica Mapfre de Medicina del Tenis, C/ Muntaner 40, 08011 Barcelona, Spain e-mail: [email protected] C. Pedret Centre de Diagnòstic per Imatge de Tarragona, Tarragona, Spain L. Capdevila Laboratory of Sport Psychology, Universitat Autònoma de Barcelona, Barcelona, Spain X. Alomar Clínica Creu Blanca, Barcelona, Spain D. A. Bong Instituto Poal de Reumatologia, Barcelona, Spain

standard.” In MRI studies, 24 cases (43.7 %) had myofascial injuries that were localized in the posterior aponeurosis (PMF) in 15 cases (27.3 %) and in the anterior aponeurosis (AMF) in 9 (16.4 %). Thirty-one cases (56.3 %) were musculotendinous injuries, with 9 cases (16.4 %) in the medial aponeurosis (MMT), 11 cases (20 %) in the lateral aponeurosis (LMT), and 11 cases (20 %) in the central tendon (CMT). In comparison to MRI, ultrasound was able to detect injury to the soleus in 27.2 % of cases. No injuries were detected by ultrasound alone. Posterior myofascial injuries were more likely to be detected by ultrasound than anterior myofascial injuries or all types of musculotendinous injuries. Ultrasound patterns for each type of injury were described. Conclusion Ultrasound is not a sensitive technique for detecting and assessing soleus traumatic tears compared with MRI, although the sensitivity is enhanced by a thorough anatomically based ultrasound examination. Timing of the ultrasound examination may be of importance. Each type of soleus injury appears to have a characteristic ultrasound pattern based on a defect of connective expansions, the existence of small myofascial filiform collections, and the rarefaction of the fibrillar area. Keywords Soleus . Ultrasound . MRI . Muscle injury

Introduction The soleus muscle is part of the superficial posterior compartment of the leg. Along with the two heads of the gastrocnemius and the plantaris muscle, it forms the calf muscle [1]. From a functional standpoint, the soleus, along with the gastrocnemius, activates plantar flexion of the ankle [2]. Ninety-six per cent of soleus muscle fibers are type I [3], functioning to maintain posture and other low-energy activities, such as walking. Since it is also a monoarticular muscle,

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acting across one joint, it might be suspected of having minimal susceptibility to musculotendinous lesions [4]. This is not the case. The soleus muscle is located on the posterior margins of the tibia and fibula, as well as within the deep fascia of the leg. It has medial and lateral intramuscular aponeuroses [5] that start at the anterior epimysium and run distally to the interior of the muscle body [4, 6]. In its central portion, there is an intramuscular tendon that reaches the Achilles tendon, contributing to its formation [7]. This complex “myo-connective system” explains the muscle’s multipennate structure [8–10] and also predisposes it to injury at the level of any of its musculotendinous junctions [11]. The soleus muscle is injured while the knee is in flexion, while the gastrocnemius is injured with the knee in a more extended position. A recent study identified five sites within the soleus where strains were distributed: three musculotendinous junction sites (proximal medial strains accounting for 25.5 % of all injuries, proximal lateral strains for 12.7 %, and distal central tendon strains for 18.2 %) and two myofascial sites (anterior strains 21.8 % and posterior strains 21.8 %; Fig. 1). Strains of the proximal medial musculotendinous junction were the most common type of soleus muscle injuries (56.4 % of all cases) [4]. Owing to the gradual onset of the injury and the fact that it is usually well tolerated [12], it is felt that the frequency of soleus lesions is underestimated. Soleus injuries are easily detected on MRI [13], but, owing to their good prognosis and the expense of MRI, it tends to be recommended only for high-level athletes [14]. Furthermore, the traditional use of ultrasound for calf injuries may under-diagnose soleus involvement because the muscle is deep, multipennate, and often extensively vascularized. These factors contribute to making ultrasound visualization difficult [13]. The objectives of this article are to assess the sensitivity of ultrasound in the diagnosis of soleus muscle injuries, using MRI as the gold standard, to perform an inter-observer ultrasound reliability study of the detection of these lesions, and to describe the varied ultrasound appearances of these lesions.

Fig. 1 Diagram of the connective muscle structure of the soleus muscle. MA medial aponeurosis, LA lateral aponeurosis, CT central tendon, PF posterior fascia, AF anterior fascia, dashed arrows axial cut level

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Materials and methods Ultrasound and MRI studies were performed on all patients who presented to the Medical Services Clinic of the Catalan Sport Council between May 2009 and February 2013 with their first episode of sharp pain that was compatible with calf strain involving the soleus muscle [12]. The investigators performing the MRI and ultrasound studies were unaware of the results of the other test. The MRI results were considered the gold standard. Other data obtained included age, weight, and height, the participant’s sport, and the number of days after the time of the injury needed to obtain testing. The ultrasound examinations were performed 2 to 31 days after the injury and the MRI during the week after the ultrasound. Magnetic resonance imaging was conducted using a highresolution 3.0-T MRI scanner (Magnetom VERIO, Siemens Medical Solutions), with a maximum gradient strength of 45 mT/m, a rise time of 225 μs, and 32 receiver channels. Image acquisition was performed using a cardiac coil with 32 elements. Coronal and axial turbo spin echo (TSE) T1-weighted sequences (TR 1,200 ms, TE 20–25 ms, SL 2.5–3 mm, in-plane resolution, 448×358 matrix, echo train length 4, FOV 350× 300 mm) and axial, sagittal, and coronal TSE fat-saturatedT2weighted sequences (TR 5,000 ms, TE 30–35 ms, SL 2–3.5 mm in-plane resolution, 350×280 matrix, echo train length 4, FOV 350×300 mm) were performed. The studies were performed and reviewed by a radiologist (XA) with more than 25 years of experience in performing musculoskeletal MRI. Ultrasound studies were performed using two machines: the Toshiba Medical Systems model SSA-770, Aplio 80 XV (Nasu, Japan), and the Toshiba Medical Systems model TUSA400, Aplio 400 (Nasu, Japan). A high-frequency linear transducer was employed with a 5- to 12-MHz probe model, PLT 805AT, with a transducer length of 67 mm and a viewing width of 58 mm. The ultrasounds were performed by two sonologists, each with more than 20 years of experience in musculoskeletal ultrasound. The entire soleus muscle was examined in both the affected and uninvolved legs along the short and long axes. in gray-scale and on color Doppler, and video clips were recorded. Muscle characteristics evaluated included: complex structure, fibrillar arrangement, and echogenicity. In cases where an injury was observed on ultrasound, the location of the lesion and whether it was a musculotendinous or myofascial injury was recorded along with a detailed description including the presence of a fluid collection (anechoic pattern), the arrangement of the aponeuroses of the soleus, alterations in the fibrillar pattern, and the existence of areas of increased echogenicity. An inter-observer reliability study was also performed by two blinded expert sonographers (RB and GR), who independently and retrospectively reviewed ultrasound static images and video clips of the MRI-positive patients.

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The software SPSS for Windows (V20, IBM) was used for standard statistical methods. One-way analysis of variance was used to compare indexes between groups and Pearson’s Chi-squared test was performed to compare distributions of percentages between group variables.

Table 2 Days (mean and SD) between the injury and the diagnostic test, depending on location and ultrasound viewing. AMF anterior myofascia, PMF posterior myofascia, MMT medial musculotendinous, CMT central musculotendinous, LMT lateral musculotendinous (0: ultrasound negative; 1: ultrasound positive) Location

Ultrasound

Mean

Standard deviation (SD)

n

AMF

0

12.40

9.501

10

1 Total 0 1 Total 0 1 Total 0 1 Total 0 1 Total 0 1 Total

28.00 17.60 10.50 29.80 21.22 2.13 31.00 5.33 27.50 31.00 27.82 6.88 27.00 12.36 12.83 28.80 17.18

29.206 18.965 12.583 21.288 19.734 3.643 – 10.210 19.840 – 18.851 10.063 18.520 15.095 15.198 20.595 18.120

5 15 4 5 9 8 1 9 10 1 11 8 3 11 40 15 55

Results Fifty-five cases of soleus injury (22 involving the right leg and 33 the left leg) were identified by MRI. Mean age was 35.6 years (range, 32.8–38.3), mean height was 178.6 (±5.2) cm and mean weight was 76.9 (±6.6) kg. All patients were athletes: 18 soccer players, 24 athletes were runners (long and medium distance running and triathlon), 12 were tennis players, and 1 was a basketball player.

PMF

MMT

CMT

Injury distribution Based on the MRI study, the cases were divided into five types of injuries according to the recent classification proposed by Balius et al. [4]. Twenty-four cases (43.7 %) had myofascial injury localized in the posterior aponeurosis (PMF) in 15 cases (27.3 %) and in the anterior myofascial injury AMF in 9 cases (16.4 %). Thirty-one patients (56.3 %) had musculotendinous strain, with 9 cases located (16.4 %) in the medial aponeurosis (MMT), 11 cases (20 %) in the lateral aponeurosis (LMT) and the final 11 cases (20 %) in the central tendon (CMT). Ultrasound study The ultrasound examination identified the “myo-connective” injury in 15 of the 55 cases (27.3 %), with 10 myofascial strains (66.7 %) and 5 musculotendinous strains (33.3 %). Of note, in the 40 negative cases, the majority were myotendinous (65 %); 35 % were myofascial. A Pearson’s Chi-squared test showed significant differences for these percentages (χ2(55.1) =4.44; p= 0.036). Within the myofascial injury group, those that were

Table 1 Distribution of soleus injuries broken down by injury location in the posterior myofascia (PMF), with respect to all other injuries in other locations, according to the ultrasound diagnosis (0: ultrasound negative; 1: ultrasound positive). * Percentage differences are significant (χ2(55.1)=4.34; p=0.05) Ultrasound

PMF REST

Injuries Percentage Injuries Percentage

Total

0

1

4 44.4 36 78.3

5 55.6 10 21.7

9 100.0 46 100.0

LMT

Total

anterior (AMF) were negative in 10 cases (66.7 %), while 5 cases (33.3 %) were positive. When the injury was posterior (PMF), 4 cases (44.4 %) were negative and 5 (55.6 %) positive. With respect to the myotendinous lesions, if the injury was located on the central tendon (CMT), only 1 case (9.1 %) was positive and the other 10 (90.9 %) were negative. For injuries located on the medial aponeurosis (MMT), 8 cases (88.9 %) turned out to be negative and only 1 (11.1 %) positive, while out of the injuries to the lateral aponeurosis, 8 cases (72.7 %) were negative and 3 (27.3 %) were positive. No significant differences were seen between these percentages, according to the Pearson’s Chi-squared test. When comparing the PMF group (4 negative and 5 positive cases) with all other cases (36 negative and 10 positive), a Pearson’s Chi-squared test revealed significant differences for

Table 3 Concordance table in ultrasound interpretations by two independent observers (0: ultrasound-negative; 1: ultrasound-positive) Concordance

Number of ultrasounds

Agreement of 0 Agreement of 1 Variance Total

8 25 11 44

Percentage concordance 18.2 56.8 25.0 10.0

75.0 25.0 100.0

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Fig. 2 MRI and ultrasound studies in a 46-year-old medium-distance runner who experienced posteromedial calf pain demonstrate posterior myofascial strain injury of the medial aspect of the soleus. a Sagittal T2weighted fat-saturated and b axial T2-weighted fat-saturated MRI showing a hemorrhage extending through the epimysium myofascial perimeter (arrows) and edema in the soleus muscle. c Axial T1-weighted MRI

showing the integrity of the plantaris tendon (arrow). d Long-axis and e short-axis ultrasound scans showing a filiform and hyperechoic hematoma (asterisk) between the medial head of the gastrocnemius and soleus muscle. Observe the integrity of the aponeurosis of the medial head of the gastrocnemius

the percentages observed. This is because for the PMF group, 55.6 % of cases were diagnosed as positive, while this percentage was only 21.7 % for all other groups (χ2(55.1) =4.34; p=0.05; Table 1).

A one-way variance analysis showed significant differences with regard to the number of days it took to perform the ultrasound between the 15 cases diagnosed as positive on the ultrasound (28.8±20.6 days) and the 40 cases diagnosed as

Fig. 3 MRI and ultrasound studies in a 28-year-old professional soccer player who experienced posteromedial calf pain over a 2-month period revealing anterior myofascial strain injury. a Axial T2-weighted, fatsaturated and b sagittal T2-weighted, fat-saturated MR images showing a clear hematoma in the anterior myofascial area (asterisks) with

surrounding edema with a feather-like arrangement consistent with a grade II strain injury. c Comparative short-axis and d comparative long-axis ultrasound scans showing a fibrillar defect (arrowheads) with an adjacent edema (asterisks) in the anterior myofascial area of the soleus muscle

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Fig. 4 Ultrasound studies with a 28-year-old professional soccer player with posteromedial calf pain with a 2-month evolution. a Ultrasound on the day of injury: note thickening with a fibrillar defect (arrowheads) and edema (asterisks) of the soleus muscle. b Ultrasound follow-up at 12 days, with the almost complete disappearance of the ultrasound injury pattern of the soleus muscle

negative (12.8±15.2 days) (F(53.1)=9.87; p=0.003). Table 2 depicts the number of days according to the location of the injuries. Reliability test The inter-observer ultrasound reliability study revealed agreement of 75 %. Of this total concordance percentage, 52.8 % corresponded to agreement on a positive ultrasound diagnosis, while 18.2 % agreed on a negative ultrasound diagnosis. A total diagnostic discrepancy percentage was observed in 11 cases (25 %; Table 3).

Fig. 5 MRI and ultrasound studies of a 32-year-old professional tennis player 1.5 months after onset of acute posterior–medial calf pain of his left leg. a Axial T2-weighted, fat-saturated and b coronal T2-weighted fat-saturated MR images showing a disruption (arrows) in the medial aponeurosis with a feather-like arrangement around it consistent with a grade II strain injury (asterisks). c Short-axis and d comparative short-axis ultrasound scans showing a fibrillar defect (arrow) with adjacent edema (asterisk) in the medial aponeurosis of the soleus muscle (arrow)

Discussion There are few studies specifically evaluating injuries to the soleus muscle in the international literature [1, 4, 13, 15, 16]. Koulouris et al. [13], in a retrospective study using MRI in a group of 59 patients with calf muscle injuries, found a high incidence of soleus involvement, with 18 soleus injuries in 39 patients with solitary lesions (46.2 %) and 16 soleus injuries in the 20 patients with dual injuries (80 %). However, Delgado et al. [15] found only a single case of soleus muscle injury in a retrospective study using ultrasound in a series of 141 cases that were seen clinically for tennis leg.

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Fig. 6 MR and ultrasound studies in a 29-year-old tennis player who experienced acute posterior calf pain with a 15-day evolution in his left leg. a Axial T2-weighted, fat-saturated and b sagittal T2-weighted, fatsaturated MR images showing a focal area of hyper-intensity centered at the middle and distal thirds of the central tendon (arrows), with intramuscular foci of hemorrhage consistent with a grade II strain injury. c Short-axis and d comparative short-axis ultrasound scans showing a moderate area of edema surrounding the central tendon (asterisk) of the soleus muscle

Based on detailed anatomical knowledge of the most likely areas of injury to the “myo-connective” junctions, we were able to identify injury to the soleus using ultrasound in 27.3 % of patients diagnosed with definite soleus involvement by MRI, with a relatively high inter-observer reliability (75 %). Despite the limitations of the ultrasound in identifying soleus injuries, it continues to be the method of choice for assessing tennis leg injuries [17] because of its accessibility, its cost compared with MRI [18, 19], and, particularly relevant, its capacity to diagnose gastrocnemius injuries, with the possibility of monitoring the injury and identifying possible Fig. 7 MR and ultrasound studies with a 25-year-old professional soccer player 7 days after the onset of acute posterolateral calf pain in his left leg. a Axial T2-weighted, fat-saturated and b sagittal T2weighted, fat-saturated MR images showing a disruption (arrows) in the medial aponeurosis, with edema with a feather-like arrangement around it, consistent with a grade II strain injury (asterisks). c short-axis and d comparative short-axis ultrasound scans showing a fibrillar defect (arrows) with moderate hypo-echogenicity adjacent to the area of the lateral aponeurosis (arrows) of the soleus muscle

complications, such as delayed myofascial hematoma or the appearance of deep vein thrombosis. Despite the relatively poor sensitivity of ultrasound in identifying soleus lesions, a number of authors feel that the use of MRI is not cost-effective [16]. Thus, MRI would only be recommended in cases in which there is a clinical diagnosis compatible with calf injury, and in which a thorough ultrasound study does not identify any injury, especially in high-performance sports, where a rapid and accurate diagnosis is required. The time between injury and the ultrasound study may be relevant in that this period in negative cases lasted 12.8 days

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compared with 28.8 days in positive cases (p=0.003). This suggests that when the evolution of the injury is more indolent it might be more readily identified by ultrasound, whereas when the progression of the fibrillar injury is more rapid, the injury is very rarely visualized. In these cases, when it is visualized, the injury is characterized by increased echogenicity, which coincides with the painful area indicated by the patient and also, at times, with small hematomas or small-caliber fibrillar defects. Also, ultrasound sensitivity appears to be dependent on the location of the injury. We observed that injuries located at the myofascial junctions (10 out of 24 or 41.7 %) are more readily identified than those situated at the musculotendinous junctions (5 out of 26 or 16.1 %). This may be due to the presence of a fluid collection that appears to facilitate ultrasound visualization of myofascial injuries. Of the myofascial injuries, PMF injuries were most easily visualized by ultrasound (p=0.05) with an ultrasound pattern consisting of an aponeurotic anechoic or hyperechoic filiform defect in the vicinity of the gastrocnemius muscle, where the aponeurosis of this muscle was intact. At this level, on occasion, it was difficult to differentiate PMF injury from plantaris tear as the ultrasound image shows a small myofascial hematoma (Fig. 2). Anterior myofascial injuries were found in the deep posterior compartment, making visualization difficult. The five positive ultrasound cases (5 out of 15) had a period of time before the examination of 29.2 days, with ultrasound revealing the existence of poorly delimited hyperechoic edema in the anterior aspect of the soleus muscle, associated, at times, with a fibrillar defect (Fig. 3). This time period suggests that these lesions might only have become visible if their evolution were rather indolent. Furthermore, these cases raised the possibility of injury involving the intramuscular septa. A followup examination at 12 days is shown in Fig. 3 and was very illustrative. We see how after diagnosing the injury and prescribing sport rest for the patient, the increased echogenicity that was noted on the first ultrasound had completely disappeared (Fig. 4). Thus, it might be concluded that the ultrasound findings of many soleus injuries disappear quickly with the sport rest, thus contributing to difficulty in making a diagnosis by ultrasound. Only 1 case of an MMT injury was identified by ultrasound at 31 days after injury (1 out of 11). An interruption of the medial aponeurosis was identified, with a small hypoechoic disruption of the surrounding ultrasound pattern, was noted with evidence on the short-axis compared with the long-axis image (Fig. 5). Similarly, only 1 case of CMT injury (1 out of 11) was identified 31 days after injury. Despite having a readily identifiable central tendon on ultrasound, the parallel orientation of the ultrasound beam to this structure makes interpreting any alterations extraordinarily difficult. In the

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single case observed on ultrasound, there was discrete rarefaction of the ultrasound pattern at the level of the middle area of the central tendon on the short axis that was not seen on the long axis (Fig. 6). Three cases of LMT injuries (3 out of 11) were identified, with an average delay time of 27 days. An interruption of lateral aponeurosis was identified with a small hypoechoic disruption of the surrounding fibrillar pattern. The short-axis section proved to be more effective for viewing the injury than the long axis (Fig. 7).

Conclusions Ultrasound is not sensitive enough to detect and assess soleus traumatic tears compared with MRI, although the sensitivity is enhanced by a thorough anatomically based ultrasound examination. The timing of the ultrasound examination may be of importance. Each type of soleus injury appears to have a characteristic ultrasound pattern based on a defect of connective expansions, the existence of small myofascial filiform collections, and the rarefaction of the fibrillar area. Conflict of interest None. Ethics approval Ethics approval was obtained from the Consell Català de l’Esport.

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Soleus muscle injury: sensitivity of ultrasound patterns.

To assess the sensitivity of ultrasound in detecting soleus muscle lesions diagnosed on magnetic resonance imaging (MRI) and to characterize their loc...
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