ORIGINAL RESEARCH published: 04 September 2020 doi: 10.3389/fphys.2020.574124 Differentiation Between Tendinous, Myotendinous and Myofascial Injuries by L-BIA in Professional Football Players Lexa Nescolarde 1* , Joaquim Terricabras 2,3 , Sandra Mechó 2,4 , Gil Rodas 2 and Javier Yanguas 2* 1 Department of Electronic Engineering, Universitat Politècnica de Catalunya, Barcelona, Spain, 2 Medical Department, Futbol Club Barcelona, FIFA Medical Center of Excelence, Barcelona, Spain, 3 Department of Surgery, Faculty of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain, 4 Department of Radiology, SCIAS–Hospital de Barcelona, Barcelona, Spain Purpose: To differentiate by localized bioimpedance (L-BIA) measurements 24 h after injury, between tendinous, myotendinous junction (MTJ), and myofascial junction (MFJ) injuries, previously diagnosed by MRI exam. To evaluate by L-BIA, the severity of MTJ Edited by: injuries graded from 1 to 3, and to determine the relationship between days to return to Emiliano Cè, play (RTP) and L-BIA measurements. University of Milan, Italy Methods: 3T MRI and tetra polar L-BIA was used to analyzed 37 muscle injuries 24 h Reviewed by: Stefano Longo, after injury in 32 male professional football players, (23.5 ± 1.5 kg m−2 ; 1.8 ± 0.1 m; University of Milan, Italy 20–30 year.) between the 2016–2017 and 2017–2018 seasons. Muscle injuries were Rod Whiteley, Aspetar Hospital, Qatar classified by The British Athletics Muscle Injury Classification (BAMIC). Percentage *Correspondence: difference of L-BIA parameters [resistance (R), reactance (Xc), and phase angle (PA)] Lexa Nescolarde of the injured side were calculated considering contralateral non-injured side as the lexa.nescolarde@upc.edu reference value. Javier Yanguas xavier.yanguas@fcbarcelona.cat Results: According to BAMIC classification and by MRI exam, we found tendinous Specialty section: (n = 4), MTJ (n = 26), and MFJ (n = 7) muscle injuries. In addition, MTJ injuries were This article was submitted to grouped according to the severity of injury in grade 1 (n = 11), grade 2 (n = 8), and Exercise Physiology, grade 3 (n = 7). Significant decrease (P < 0.01) was found in the L-BIA parameters R, a section of the journal Frontiers in Physiology Xc, and PA, in both MTJ and MFJ as well as in the different grades of MTJ injuries. Received: 18 June 2020 In particular, in Xc (P < 0.001), which is related to muscle cell disruption. Regarding Accepted: 14 August 2020 days to RTP, there was statistical significance among the three different grades of MTJ Published: 04 September 2020 injuries (P < 0.001), especially when grade 1 was compared to grade 3 and grade Citation: Nescolarde L, Terricabras J, 2 compared to 3. Mechó S, Rodas G and Yanguas J Conclusion: L-BIA is a complementary method to imaging diagnostic techniques, such (2020) Differentiation Between Tendinous, Myotendinous as MRI and US, to quantify MTJ and MFJ injuries. In addition, the increase in the severity and Myofascial Injuries by L-BIA of the MTJ injury resulted in higher changes of the Xc parameter and longer time to RTP. in Professional Football Players. Front. Physiol. 11:574124. Keywords: localized bioimpedance, MRI, myotendinous junction, grade of muscle injury, professional doi: 10.3389/fphys.2020.574124 football players Frontiers in Physiology | www.frontiersin.org 1 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA INTRODUCTION soft tissue, and reactance (Xc) associated with the integrity of soft tissue structures (Lukaski, 1996; Lukaski and Piccoli, 2012, Muscle injures of lower limbs are the most common injury Lukaski, 2013). The current is delayed by the current flowing types in athletes (Junge et al., 2009; Engebretsen et al., 2013), through the cell membranes (capacitive element, C). The Xc = 1 accounting for more than 30% of injuries in professional football 2πfC is an indirect measure of the amount of applied current that players (Ekstrand et al., 2011; Elliott et al., 2011). This trend seems penetrates to the cell membranes (Lukaski et al., 2019). That is, to keep growing in professional male football players in Europe bioimpedance is a p complex number Z = R−jXc, whose module, (Ekstrand et al., 2016). Z is obtained by (R)2 + (Xc)2 and phase angle (PA) is the An optimal diagnosis of muscle injury determines the severity   tan−1 Xc/R . of the injury, time to return to play (RTP) and risk of re- injury. However, determining the optimal RTP in professional When bioimpedance measurements are taken on a specific football players is difficult due to the variability and complexity human body area, they are known as localized bioimpedance of the process. The decision of whether an athlete can safely RTP measurements (L-BIA). One of the first clinical applications remains challenging (Askling et al., 2010) with ∼ 60% of re- of non-invasive L-BIA at 50 kHz is related to electrical injuries few weeks after RTP (Brooks et al., 2006; Heiderscheit impedance myography (EIM) in neuromuscular diseases et al., 2010). Imaging, either through magnetic resonance imaging demonstrated significantly reduced values of R, Xc, and PA (MRI) and/or ultrasound imaging (US) is key to assess muscle due to muscle fiber atrophy, connective tissue accretion, injuries and prognosis. However, it is still debated whether MRI fat infiltration, and edema (Rutkove et al., 2008; Rutkove, report is a good predictor for time to RTP (Reurink et al., 2014). 2009). Lukaski and Moore (2012), using L-BIA with phase- This is probably due to the lack of consensus in the diagnosis and sensitive BIA analyzer at 50 kHz, identified in lower leg classification of muscle injuries. wounds, a moderate decrease in R, Xc, and PA acutely In the last 8 years, there have been proposed multiple after removing damaged tissue from a wound. Notably, different systems of muscle injury classifications based on clinical the decreased occurred during infection and R, Xc, and examination and radiological findings, especially through MRI PA values were restored after healing. Therefore, L-BIA (Mueller-Wohlfahrt et al., 2013; Pollock et al., 2014; Valle could provide a safe and effective method to detect changes et al., 2017). The British Classification of Muscle Injuries of at cellular level. Athletics, BAMIC (Pollock et al., 2014), based on MRI findings, In professional football players (Nescolarde et al., 2013, is one of the most internationally used and classifies muscle 2015), L-BIA measurements using 50 kHz phase-sensitive BIA injuries according to anatomical location: myofascial, muscle- analyzer, are in agreement with the severity of muscle injury, tendon junction, and intratendinous; as well as according to diagnosed by MRI 24 h after injury, according to muscle gap the severity of the injury, grading from 0 to 4. Moreover, and independently to anatomical location. L-BIA measurements the BAMIC specifies that each hamstring muscle injury 24 h after injury showed a significant reduction of R, Xc and localization has different RTP. The criteria is based on the PA directly related to the severity of muscle injuries, being tissue type involved and the extent of the injury, being the more noticeable in Xc than in R. Moreover, more severe intratendinous injury the one with longer time to RTP and injuries showed larger percentage difference in Xc (% difference) higher recurrence rate (Patel et al., 2015; Pollock et al., 2016; (Nescolarde et al., 2013, 2015). Sometimes there is a great Wangensteen et al., 2017). challenge for the sports physicians and radiologists to be able The classification proposed by Pollock et al. (2014) agree with to confirm diagnosis and especially the prognosis. Accurately the idea of a histoarchitectural approach to skeletal muscle injury quantifying the severity of muscle injury could help to improve from Balius et al. (2020) describing that when myoconnective the diagnosis of muscle injury. junction is affected, the injury can be located either in a MTJ This work aims (1) to differentiate by L-BIA, according to (the injury affects an aponeurosis or a tendinous expansion anatomical location, between tendinous, MTJ and MFJ injuries, attached to muscle fibers) or in the myofascial junction (MFJ) previously diagnosed by MRI exam 24 h after injury; (2) to (when the injury involves muscle fiber and their perimysium determine the severity of MTJ injuries graded from 1 to 3 by and/or epimysium). And when an injury in the myoconnective L-BIA; and (3) to determine the relationship between days to junction has a tendon gap (by MRI), the injury will have return to play (RTP) and L-BIA measurements 24 h after injury worst prognosis, require longer time to RTP and could present with severity of the injury. greater risk of re-injury compared to others injuries. However, a study of full-thickness intramuscular tendon damage, did not show re-injury after 12 months (Vermeulen et al., 2019). MATERIALS AND METHODS Regarding MTJ and MFJ injuries, it is not clear which one has better prognosis and, consequently, less time to RTP Participants (Balius et al., 2020). Futbol Club Barcelona (FCB) Medical Department studied Mono-frequency non-invasive electrical bioimpedance is prospectively 37 muscle injuries of 32 male professional associated with the injection of low-intensity sinusoidal current football players, (23.5 ± 1.5 kg m−2 ; 1.8 ± 0.1 m; 20– at 50 kHz into a biological conductor resulting in measuring 30 year.) between the 2016–2017 and 2017–2018 seasons values of resistance (R), associated with the hydration state of to assess and compare L-BIA and MRI findings. This Frontiers in Physiology | www.frontiersin.org 2 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA study only evaluates injuries of football players (both approach to skeletal muscle injury (Balius et al., 2020) taking during matches and training sessions) that presented acute to account: muscle injury, to whom the medical team prescribed 1. Myoconnective junction affected an MRI in the first 24 h after the injury, and in those cases that L-BIA study was performed during the  Tendinosis injuries are tears that extend into the tendon. same period of time.  Myotendinous junction (MTJ) injuries are high signal change occurs within the muscle or more commonly located exactly at the MTJ. Magnetic Resonance Imaging (MRI)  Myofascial junction (MFJ) injuries extend from Magnetic resonance imaging is not only the gold standard the fascia and demonstrate high signal change technique of choice in professional football for diagnosing on fat-suppressed/STIR sequences within the muscle injuries that has proven to be an essential tool periphery of the muscle. in the assessment of muscle injuries in elite athletes, but is also rapidly becoming the imaging technique of 2. Severity of the injury, graded from 1 to 4 choice for the evaluation of the connective tissue injuries (Schneider-Kolsky et al., 2006; Ekstrand et al., 2012).  Grade 1 injuries are small tears. High signal in MRI extends This imaging technique allows specialists to define muscle less than 10% of the cross-sectional area (CSA) of the injury with excellent resolution of the three axes, including muscle and over a limited area of less than 5 cm. oblique planes, and assessing deep muscles by identifying  Grade 2 shows hyper signal in MRI measure between 10 and the injury site from the origin, proximal myotendinous 50% of CSA or extends between 5 and 15 cm within the junction, muscle belly, distal junction or insertion point muscle with a fiber disruption (gap) less than 5 cm. (Ahmad et al., 2013).  Grade 3 injuries show high signal change patterns greater than 50% of the CSA or greater than 15 cm in length.  Grade 4, complete muscle or tendon tears are not MRI Protocol included in this study. Magnetic resonance imaging was performed on 3T Canon Vantage Titan (Canon Medical Systems, Japan) in FCB Medical Center by a specialist musculoskeletal radiologist (SM) to classify the muscle injury. The specific MRI paramentrs are a maximum gradient strength of 45, 203 T/m/s Slew Rate, and 32 receiver channels. Axial, Sagittal and Coronal T2 Fat Sat, TR 5200, 5000, and 3700 ms, TE 44–60 ms, Eco train 7.5, SL 2.5–3.5 mm, in-plane resolution 0.9–1.4 mm× 0.88– 0.97 mm, FOV 256 × 256, 192 × 272, 288 × 320 mm, and Axial and Coronal TSE T1, TR 900–980 ms, TE 11 ms, Eco train 7.5, SL 2.5–3.5 mm, in-plane resolution 0.71– 0.9 mm × 0.71–0.9 mm, FOV 352 × 352, 288 × 320 mm was acquired. On T2 Fat Sat sequences, muscle injuries are detected by the presence of hyperintense fluid accumulation. It is recommended to perform fluid-sensitive sequences (T2- weighted in our case) with intermediate echo time (TE) (e.g., less than 65 ms) to obtain an adequate contrast and spatial resolution of connective tissues. With these sequences we are able to detect edematous changes around the myotendinous, myoaponeurotic, and myofascial junctions, identify small tears in the connective tissue, as well as to delineate intra- or inter-muscular fluid collections or hematomas. T1-weighted sequences are useful in the assessment of hematic collections, in the detection of fatty muscular infiltration, as well as in the detection of scar tissue in chronic injuries that could be detected as chemical shift artifacts in the T2- weighted sequences. Muscle Injury Grouping Through MRI Exam 24 h After Injury After MRI exam, 37 muscle injuries were categorized FIGURE 1 | Tetra-polar L-BIA electrode placement for intramuscular septum according to The British Athletics Muscle Injury Classification rectus femoris (MTJ). (Pollock et al., 2014) and considering the histoarchitectural Frontiers in Physiology | www.frontiersin.org 3 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA FIGURE 3 | Proximal MTJ injury of rectus femoris [connective tissue tear (arrow), and muscle fibers damaged with loss of pennation angle] in axial (A) and sagittal (B) T2 weighted fat suppressed images. FIGURE 2 | Tendinous injury of the central tendon of rectus femoris (longitudinal tear of the central tendon with slight peritendinous edema) in axial (A) and coronal (B) T2 weighted fat-suppressed images. Localized Bioimpedance Measurements (L-BIA) Tetra polar L-BIA measurements, both in the injured side and the non-injured side, were performed 24 h after occurrence of the injury to quantify the percentage difference in R, Xc, and PA of injured side respect to the contralateral non- injured side. The impact of the severity of muscle injury was characterized by the percentage difference in L-BIA (R, Xc, and PA). All injuries were diagnosed 24 h after injury by MRI exam. The variability of R and Xc (Nescolarde et al., 2015) FIGURE 4 | Distal MFJ injury of rectus femoris (arrow) in axial (A) and coronal between left and right non-injured muscle area were studied (B) T2 weighted fat-suppressed image. in 10 non-injured football players on three different days with an interval of 7-day between each measurement. The intra- individual differences in 1/3 proximal quadriceps, 1/3 medium quadriceps, 1/3 proximal hamstrings and 1/3 medium hamstrings was evaluated by 5 examiners. The range of variability was ranged from −2.1 to 0.5  and the inter-individual differences negligible, 1  for R and 0.45  for Xc. The mean ± SD were lower than 15% (2 SD). value of R and Xc were 39.6 ± 0.6 and 14.2 ± 0.5  The measurements were taken with a phase-sensitive respectively, with coefficients of variation of 1.4% for R impedance instrument BIA 101 Anniversary (Akern-Srl, and 3.2% for Xc. Florence, Italy) that applied a constant sinusoidal alternating In injuries located near the bone detector, voltage electrodes current of 245 µARMS at 50 kHz. The range of measure for were placed 10 cm proximally and 10 cm distally, respectively, resistance is 0–1500  and for reactance 0–500 , with 2% from the center of the injury to increase the sensitivity of the maximum tolerance. Measurement errors determined with a measurement (Sanchez et al., 2016; Rutkove et al., 2017). parallel circuit of precision resistor and capacitor, were <1  for R and <2% for Xc. The adhesive contact electrode Ag/AgCl (COVIDIEN Ref. Injury Diagnosis and Return to Play 31050522, COVIDIEN llc, Mansfield, IL, United States) with Criteria R and Xc intrinsic values of 10.89 and 0.30  respectively Injuries were diagnosed by the medical team of the FCB Medical (Nescolarde et al., 2016), was chosen for L-BIA measurements. Department based on clinical history, physical examination, Similar to previous reports (Nescolarde et al., 2015, 2017) and US and MRI assessment. The establishment of return detector voltage electrodes (red) were placed 5 cm proximally to play (RTP) criteria was addressed by the FCB Medical and 5 cm distally, respectively, from the center of the Department and team physicians follow the criteria expressed injury located by US Aplio i800 (Canon Medical Systems, in FCB Muscle Guide 2019 (Barça Innovation Hub, 2020). Japan). Two current injecting electrodes (black) were The RTP (in days) started when the injury occurred and placed close to the detector voltage electrodes (Figure 1). continued beyond the point when the player made his return Because of the proximity of the current-introducing and to unrestricted match play (Hägglund et al., 2005). The voltage-detecting electrodes, the inter-tester reproducibility RTP plan of FCB is individual avoiding re-injuries due to (Nescolarde et al., 2013) of the R and Xc measurements premature reinstatements. Frontiers in Physiology | www.frontiersin.org 4 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA TABLE 1 | Individual values of L-BIA measurements 24 h after injury [contralateral non-injured side (1), injured side (2) in R, Xc, and PA], including tendinous (n = 4), MTJ (n = 26), and MFJ (n = 7) injuries. Muscle R () Xc () PA (◦ ) Injuries Anatomical Non-injured side Injured side 24 h Non-injured side Injured side 24 h Non-injured side Injured side 24 h location 24 h after injury (1) after injury (2) 24 h after injury (1) after injury (2) 24 h after injury (1) after injury (2) 1 T1 33.5 32.4 13.9 13.8 22.5 23.1 2 T2 38.8 38.0 17.2 17.0 23.9 24.1 3 T3 39.4 39.7 13.2 13.2 18.5 18.4 4 T4 45.5 44.4 12.8 12.8 15.7 16.1 5 MTJ-Grade 1 32.0 29.0 16.0 14.0 26.6 25.8 6 MTJ-Grade 1 29.0 26.0 14.0 12.0 25.8 24.8 7 MTJ-Grade 1 47.0 43.0 18.0 16.0 21.0 20.4 8 MTJ-Grade 1 31.0 28.0 15.0 13.0 25.8 24.9 9 MTJ-Grade 1 37.4 34.6 14.0 11.9 20.5 19.0 10 MTJ-Grade 1 48.7 41.5 15.0 12.6 17.1 16.9 11 MTJ-Grade 1 35.8 31.8 12.0 10.6 18.5 18.4 12 MTJ-Grade 1 42.0 40.1 18.9 17.5 24.2 23.6 13 MTJ-Grade 1 53.6 52.1 11.2 9.8 11.8 10.7 14 MTJ-Grade 1 39.1 37.1 15.7 14.5 21.9 21.3 15 MTJ-Grade 1 49.0 47.4 15.9 13.7 18.0 16.1 16 MTJ-Grade 2 42.0 37.0 17.0 13.0 22.0 19.4 17 MTJ-Grade 2 34.0 32.0 13.0 10.0 20.9 17.4 18 MTJ-Grade 2 38.6 35.0 15.2 12.0 21.5 18.9 19 MTJ-Grade 2 44.8 38.5 17.3 13.6 21.1 19.5 20 MTJ-Grade 2 59.4 52.0 14.2 11.2 13.4 12.2 21 MTJ-Grade 2 32.3 32.2 13.4 11.5 22.5 19.7 22 MTJ-Grade 2 41.0 38.0 13.2 11.0 17.8 16.1 23 MTJ-Grade 2 32.1 29.1 13.5 11.5 22.8 21.6 24 MTJ-Grade 3 29.3 24.6 15.3 9.7 27.5 21.6 25 MTJ-Grade 3 44.0 36.0 14.0 10.0 17.7 15.5 26 MTJ-Grade 3 39.6 27.7 14.3 7.3 19.8 14.6 27 MTJ-Grade 3 43.3 34.4 20.8 12.2 25.7 19.5 28 MTJ-Grade 3 42.9 40.3 12.9 9.8 16.7 13.7 29 MTJ-Grade 3 32.0 27.0 13.4 10.3 22.7 20.9 30 MTJ-Grade 3 43.2 37.6 16.7 12.3 21.1 18.1 31 MFJ 37.6 28.9 12.7 9.5 18.7 18.2 32 MFJ 68.0 54.0 19.0 13.0 15.6 13.5 33 MFJ 29.3 25.4 13.4 9.3 24.6 20.1 34 MFJ 37.2 32.4 15.0 11.1 22.0 18.9 35 MFJ 34.7 27.6 16.8 9.2 25.8 18.4 36 MFJ 47.3 40.4 18.5 12.7 21.4 17.5 37 MFJ 32.9 24.3 15.1 8.2 24.7 18.6 R, Resistance; Xc, Reactance; PA, phase angle; T, tendinous; MTJ, myotendinous junction; MFJ, myofascial junction. Data Analysis One-way ANOVA test was used to determine statistical The normality of distribution in the variables was determined differences in the percentage difference of R, Xc, PA, by the Shapiro-Wilk test and the homogeneity of variances and RTP values, between tendinous, MTJ, and MFJ by Levene’s test. Normally distributed variables are shown injuries, as well as between different grades of severity as mean ± SD. of MTJ injuries. Repeated measures ANOVA test 2 × 3 was used to determine Both, repeated measures ANOVA and One-way ANOVA test, statistical differences between injured side respect to non-injured with multiple comparison tests by Bonferroni (homogeneity side in R, Xc, and PA considering contralateral non-injured variances assumed) or Tamhane’s T2 test (homogeneity variances side as reference value. In addition, different grades of severity not assumed) were used. (grades 1 to 3) of MTJ injuries were analyzed following the same Discriminant Function Analysis was used to find a linear statistical procedure. combination of features that separates muscle injuries L-BIA Frontiers in Physiology | www.frontiersin.org 5 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA TABLE 2 | Values of L-BIA measurements 24 h after injury [contralateral non-injured side (1), injured side (2) and % difference in R, Xc, and PA], and the result of repeated measures ANOVA test corresponding to tendinous, MTJ and MFJ. Tendinous, (n = 4) Non-injured side 24 h after injury (1) Injured side 24 h after injury (2) Difference,% F P value (1–2)a1 R () 39.3 ± 4.9 38.6 ± 5.0 −1.8 ± 1.8 4.119 0.135 Xc () 14.3 ± 2.0 14.2 ± 1.9 −0.5 ± 0.6 2.455 0.215 PA (0 ) 20.2 ± 3.7 20.4 ± 3.8 1.2 ± 1.5 2.865 0.189 MTJ, (n = 26) Non-injured side 24 h after injury (1) Injured side 24 h after injury (2) Difference,% F P value(1–2)a2 R () 40.1 ± 7.7 35.8 ± 7.4 −10.7 ± 6.3 65.640 <0.001 Xc () 15.0 ± 2.2 12.0 ± 2.2 −20.0 ± 10.1 76.565 <0.001 PA (0 ) 20.9 ± 3.9 18.9 ± 3.8 −9.9 ± 7.0 41.988 <0.001 MFJ, (n = 7) Non-injured side 24 h after injury (1) Injured side 24 h after injury (2) Difference,% F P value(1–2)a3 R () 41.0 ± 13.1 33.3 ± 10.6 −18.7 ± 5.2 38.248 0.001 Xc () 15.8 ± 2.4 10.4 ± 1.9 −33.7 ± 8.4 73.600 <0.001 PA (0 ) 21.8 ± 3.7 17.9 ± 2.1 −17.0 ± 8.4 19.509 0.004 a Repeated measures ANOVA test between non-injured side (1) and injured side (2) according to 1 tendinous, 2 MTJ, 3 MFJ injuries. R, resistance; Xc, reactance; PA, phase angle; MTJ, myotendinous junction; MFJ, myofascial junction. FIGURE 5 | Mean and SD of the % difference in R, Xc, and PA of twenty-six MTJ (red) injuries and seven MFJ (blue). Results of One-way ANOVA between % difference of MTJ respect to MFJ injuries, are also presented. values (% difference in R, Xc, and PA) according to the grade of injury, were grouped according to the myoconnective junction severity of MTJ injuries. affected and classified following Pollock et al., 2014 in tendinous The statistical software IBM SPSS version 22.0 (IBM Corp, R R (n = 4), MTJ (n = 26), and MFJ (n = 7) injuries (Figures 2–4). Armonk, NY, United States) was used for data analysis. The level These injuries affected the long head of the biceps of statistical significance was set at P < 0.05. femoris (n = 12), the short head of the biceps femoris (n = 9), rectus femoris (n = 10), semitendinosus (n = 4) and semimembranosus (n = 2). RESULTS Tendinous, MTJ and MFJ Injuries, L-BIA Measurements in Tendinous, MTJ Previously Diagnosed With MRI 24 h and MFJ Injuries Diagnosed Previously After Injury by MRI 24 h After Injury A total of 37 muscle injuries occurred between 2016–2017 and Table 1 shows the individual values of L-BIA measurements 2017–2018 seasons and evaluated by an MRI exam 24 h after 24 h after injury [resistance (R), reactance (Xc), and phase Frontiers in Physiology | www.frontiersin.org 6 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA of MTJ injuries (MTJ-Grade 1, MTJ-Grade 2, MTJ-Grade 3) are also displayed. Table 2 describes the L-BIA measurements 24 h after injury, of thirty-seven muscle injuries, as mean ± SD corresponding to tendinous (n = 4), MTJ (n = 26), and MFJ (n = 7) injuries and the percentage difference (Difference,%) in resistance (R), reactance (Xc), and phase angle (PA). In addition, the result of the repeated measures ANOVA test between injured side compared to the non-injured side of R, Xc, and PA is reported. Using repeated measures ANOVA test, anatomical changes related to tendinous injury were not reflected by L-BIA FIGURE 6 | Distal MTJ injury grade 1 of rectus femoris in axial (A) and coronal (B) T2 weighted fat-suppressed image. Small myofascial tear (arrow). measurement through R, Xc, and PA (P > 0.05), 24 h after injury. The percentage difference in R, Xc, and PA, 24 h after injury, were −0.5% ∼ −2%. However, we found statistical significance (P < 0.01) for R, Xc, and PA for both MTJ and MFJ injuries. The MTJ injury results showed statistical significance (P < 0.001) in percentage difference of R, Xc, and PA in the injured side compared to the contralateral non-injured side (−11% in R, −20% in Xc and −10% in PA), as well as MFJ injuries (P < 0.01) in percentage difference of R, Xc, and PA in injured side compared to the contralateral non-injured side (−19% in R, −34% in Xc, and −17% in PA). The One-way ANOVA test, with regard to MTJ and MFJ injuries, shows statistical significance for% difference in R (F = 9.673, P = 0.004), Xc (F = 10.775, P = 0.003) and statistical significance for PA (F = 5.155, P = 0.030). FIGURE 7 | Proximal MTJ injury grade 2 of rectus femoris in axial (A) and Figure 5 shows the mean and SD of percentage coronal (B) T2 weighted fat-suppressed image. Blurring of the muscle fibers in difference (% Difference) in R, Xc, and PA, of MTJ and the lateral MTJ of the central septum, with a small hematoma. We can see MFJ injuries, diagnosed by MRI exam 24 h after injury that this is an overloaded rectus femoris. and evaluated by L-BIA measurements. In addition, the result of One-way ANOVA between % difference of R, Xc and PA in MTJ respect to % difference of R, Xc, and PA in MFJ injuries. L-BIA Measurements of MTJ Grouped According to the Severity of the Injury Diagnosed Previously by MRI 24 h After Injury In a second analysis, 26 myotendinous junction (MTJ) injuries, evaluated by MRI 24 h after injury, were grouped according to the severity of the injury (Figures 6–8) follow BAMIC classification (Pollock et al., 2014) in grade 1 (n = 11), grade 2 (n = 8), and grade 3 (n = 7). Table 3 presents the L-BIA measurements 24 h after the injury as mean ± SD and percentage difference (Difference,%) in R, FIGURE 8 | Proximal MTJ injury grade 3 of rectus femoris in axial (A) and Xc, and PA corresponding to the grade of severity of MTJ injury coronal (B) T2 weighted fat-suppressed image. The mixed tear of the central in grade 1 (n = 11), grade 2 (n = 8) and grade 3 (n = 7). septum (transversal and longitudinal), resulting in loss of tension and extensive In addition, the result of the repeated measures ANOVA test feathery edema. between injured side compared to the non-injured side of R, Xc, and PA is presented. Using repeated measures ANOVA test, anatomical changes angle (PA)] of thirty-seven muscle injuries. According to related to the grade of MTJ injuries were reflected by L-BIA anatomical location, injuries are classified as tendinous (n = 4), measurement through R, Xc, and PA (P < 0.01), 24 h after injury MTJ (n = 26) and MFJ (n = 7) in). Grades of severity for grade 1, 2, and 3. Frontiers in Physiology | www.frontiersin.org 7 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA TABLE 3 | Values of L-BIA measurements 24 h after injury [contralateral non-injured side (1), injured side (2) and % difference in R, Xc, and PA] corresponding to the grade of MTJ injuries, and the result of repeated measures ANOVA test for R, Xc, and PA. MTJ-Grade 1, (n = 11) Non-injured side 24 h after injury (1) Injured side 24 h after injury (2) Difference,% F P value(1–2)b1 R () 40.4 ± 8.3 37.3 ± 8.4 −7.9 ± 3.7 40.405 <0.001 Xc () 15.1 ± 2.3 13.2 ± 2.3 −12.3 ± 2.8 229.221 <0.001 PA (◦ ) 21.0 ± 4.5 20.2 ± 4.6 −4.3 ± 3.3 28.279 <0.001 MTJ-Grade 2, (n = 8) Non-injured side 24 h after injury (1) Injured side 24 h after injury (2) Difference,% F P value(1–2)b2 R () 40.5 ± 9.0 36.7 ± 7.0 −8.8 ± 4.4 20.788 0.004 Xc () 14.6 ± 1.7 11.7 ± 1.1 −19.5 ± 3.7 108.784 <0.001 PA (◦ ) 20.3 ± 3.2 18.1 ± 2.9 −10.8 ± 3.5 54.428 <0.001 MTJ-Grade 3, (n = 7) Non-injured side 24 h after injury (1) Injured side 24 h after injury (2) Difference,% F P value(1–2)b3 R () 39.2 ± 6.0 32.5 ± 6.0 −17.1 ± 7.3 31.968 0.001 Xc () 15.3 ± 2.7 10.2 ± 1.7 −32.7 ± 9.8 42.505 0.001 PA (◦ ) 21.6 ± 4.0 17.7 ± 3.1 −17.8 ± 6.6 32.618 0.001 b Repeated measures ANOVA test between non-injured side (1) and injured side (2) according to grade of MTJ injuries 1 grade 1, 2 grade 2, 3 grade 3. R, resistance; Xc, reactance; PA, phase angle; MTJ, myotendinous junction; MFJ, myofascial junction. FIGURE 9 | Mean and SD of % difference in R, Xc, and PA of MTJ injury grades 1–3. SE and results from post hoc test are also presented. The One-way ANOVA test, regarding the MTJ injuries the results of Tamhane’s T2 multiple comparison test classified in grades 1, 2, and grade 3, showed statistical revealed statistical differences (P < 0.001) in Xc and significance in the % difference of R (F = 7.630, P = 0.003) PA between grade 1 and grade 2, as well as between and statistical significance for % difference of Xc (F = 26.964, grade 1 and grade 3. P < 0.001) and % difference of PA (F = 20.089, P < 0.001). Figure 10 shows the canonical discriminant functions, Figure 9 shows the mean and SD of the % difference according to the grade of MTJ injuries, by Discriminant Function in R, Xc, and PA, of twenty-six MTJ injuries classified Analysis of percentage difference (% difference) in R, Xc, and PA. as grade 1 (n = 11), grade 2 (n = 8), and grade 3 The function scores obtained through the standardized (n = 7) by MRI exam, 24-hour after injury. In addition, canonical discriminant function coefficients are: Frontiers in Physiology | www.frontiersin.org 8 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA TABLE 4 | Return to play in MTJ and MFJ injuries. Anatomical Location (Sample size) RTP, days F P value1 MTJ (26) 25 ± 22 2.277 0.124 MFJ (7) 20 ± 8 Grade of MTJ injury (Sample size) RTP, days F P value2 Grade 1 (11) 8±3 39.517 P < 0.001 Grade 2 (8) 14 ± 10 Grade 3 (7) 52 ± 14 1 One-way ANOVA between MTJ and MFJ injuries. 2 One-way ANOVA among MTJ injuries according to severity. also statistical difference (SE = 5.475, P = 0.001) contrasting grade 2 (14 ± 10 days) with grade 3 (52 ± 14 days). DISCUSSION FIGURE 10 | Canonical discriminant functions for % difference in R, Xc, and This second project of L-BIA developed by FCB Medical PA, according to the grade of MTJ injuries, of grade 1 (n = 11), grade 2 Department evaluates the capacity of the L-BIA method (n = 8), and grade 3 (n = 7). to differentiate muscle injuries according to anatomical location in tendinous, MTJ and MFJ, which are diagnosed by MRI exam 24 h after injury and classified according to The British Athletics Muscle Injury Classification (Pollock FScore1 = 3.198 % difference R − 5.093 % difference Xc et al., 2014) considering the histoarchitectural approach + 2.701 % difference PA to skeletal muscle injury (Balius et al., 2020). The most important finding is the good association between both MRI and L-BIA methods in myotendinous junction (MTJ) and FScore2 = 4.212 % difference R − 4.746 % difference Xc myofascial junction (MFJ) injuries. Also, the fact that higher changes in Xc, and longer time to RTP are found in more +3.064 % difference PA severe MTJ injuries. Comparing the injured side to non-injured side both for Both first and second function show the standardized MTJ and MFJ injuries, the % difference in L-BIA measurements coefficient for % difference R, % difference Xc, and % 24 h after injuries are in concordance with findings by difference PA. The magnitude of these coefficients indicate MRI exam 24 h after injury. The contralateral non-injured how strongly the discriminating variables affect the score. side is taken as reference due to the individual symmetry Thus, % difference in Xc has the greatest impact of the in L-BIA values between left and right muscle areas of the three variables, on the first (−5.093) and second (−4.746) lower-limb in professional football players. By MRI exam, discriminant score, but especially in the first score. Therefore, MFJ injuries show greater edema and greater bleeding than Xc is the variable that most discriminates according MTJ injuries, which justifies why the percentage difference (% to the grade of MTJ injuries by L-BIA measurements difference) of the injured side compared to the contralateral 24 h after injury. non-injured side is greater in MFJ injuries than in MTJ injuries. Both in MTJ and MFJ injuries the % difference in Return to Play (RTP) in MTJ and MFJ Xc was greater than the % difference in R. According to our Injuries findings, to evaluate anatomical changes produced in MTJ Table 4 present the RTP (in days), and the result of the One-way and MFJ, 24 h after injury by L-BIA, the Xc is the most ANOVA test between MTJ and MFJ injuries and according to the sensitive variable. grade of severity of MTJ injuries. Although the tendinous injuries are the most severe cases Using the One-way ANOVA test, and regarding MTJ and MFJ (Crema et al., 2016) L-BIA method is completely insensitive injuries, the RTP does not show statistical significance (P > 0.05). to the anatomical changes produced in the tendinous injuries. Regarding the MTJ injuries classified in grades 1, 2, and grade Fortunately, they are also less common in professional football 3, we found statistical significance in days to RTP (P < 0.001). players (Crema et al., 2016). By MRI, the tendinous injuries Tamhane’s T2 reveals statistical difference (SE = 5.121, P = 0.002) show less edema and bleeding comparing to MTJ and MFJ contrasting grade 1 (8 ± 3 days) with grade 3 (52 ± 14 days) and injuries, and the intra-tendinous gap is considerably smaller. Frontiers in Physiology | www.frontiersin.org 9 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA A normal tendon is a compact structure with tenocytes contralateral non-injured side with % difference lower than 15% attached to a highly ordered fibrillar collagen matrix (ECM) in those muscle injuries of high degree of severity according composed of type-I collagen (65–80% of its dry mass), and to the muscle “gap” (Nescolarde et al., 2013). It is important small leucine-rich proteoglycans that regulate collagen self- mentioning that for measurements on injured muscles with assembly into collagen fibrils, which in turn are ordered by L-BIA until RTP time point, each player is his own reference the cell into collagen fibers (Snedeker and Foolen, 2017). (Nescolarde et al., 2013). The role of MRI is key for the diagnosis In the intratendinous injury, tendon gap is smaller than and prognosis of injuries, and therefore, a great tool for RTP those in muscle injuries and show generally less edema and prediction. However, it is not the only criterion to take into bleeding than MTJ and MFJ injuries in MRI fluid-sensitive account. The decision on time to RTP by FCB physicians are sequences. In acute intratendinous injuries, there is no major based on club’s guidance, taking into account not only imaging inflammatory component and its repair process goes along criteria but also specific tests, GPS assessment, and even the the lines of scar formation causing to the tensile strength player’s psycho-emotional state. of healed tendon like the healthy tendon (Nourissat et al., 2015). It should be clarified that differently to the hamstring free tendon, the intramuscular tendon has more vascularization CONTRIBUTION (Brukner and Connell, 2016). Comparing the percentage difference of MTJ injuries to Localized bioimpedance is a complementary method to MRI the percentage difference of MFJ injuries, as in MRI exam and US as currently it can only quantify MTJ and MFJ 24 h after injury, both for edema produced in the area of the injuries. In addition, it could be useful for the medical injury (% difference R) and the amount of cell disruption (% team, physiotherapists, and physical trainers in the diagnosis difference Xc), the L-BIA method distinguishes between MTJ of muscle injury helping in day-to-day decision-making. and MFJ injuries. The % difference in phase angle is more L-BIA measurements are carried out using a phase-sensitive closely related to the changes produced in the Xc than with impedance instrument at 50 kHz, robust and easy to apply, and those produced in R for the geometric relationship between them economically feasible. (Lukaski, 1996; Lukaski et al., 2019). In professional football, muscle injuries occur with major frequency at the myotendinous junction (MTJ) especially in LIMITATION hamstring muscle groups (Crema et al., 2016) whose main objective is the transmission of force (Balius et al., 2018). In To validate L-BIA as a complementary method to MRI and this study, 26 out of 37 injuries occurred in the myotendinous US, it is necessary to extend this study to other professional junction, which were classified into grades 1, 2, and 3, according football teams to increase the sample size, as well as to include to the severity of the injury. All of them showed a notable female athletes. decrease in R and Xc, being the largest change observed in Xc. Furthermore, this change was even greater in grade 3 of the MTJ injury after comparing the injured side to the non-injured CONCLUSION side. The % difference of MTJ injuries grade 1 compared to the % difference of MTJ injuries grade 2 and MTJ grade 3, We conclude that L-BIA is a tool able to differentiate elucidated that the more severe the injury is, higher changes between MTJ and MFJ injuries. Additionally, it discriminates in R and Xc are found, especially in Xc which is relate to between MTJ grade 3 injury and grades 1 and 2. The muscle “gap” in agreement with the findings shown on the MRI sensitivity of L-BIA method is shown to be higher in exam 24 h after injury. Similar to wound healing (Lukaski and the percentage difference of Xc 24 h after injury, which Moore, 2012), muscle injury is classified according to anatomical is related to muscle cell disruption. In addition, more location, the % difference in Xc (cell disruption, muscle “gap”) is severe injures presented higher % difference in Xc and related with the severity of the injury. Regarding RTP (in days), longer time to RTP. it was not found differences between MTJ and MFJ injuries. However, according to severity of MTJ injuries, it was found differences among days to RTP and MTJ grades 1, 2, and 3. The DATA AVAILABILITY STATEMENT injuries with the highest degree of severity were associated with longer time to RTP. The raw data supporting the conclusions of this article will be The decision on the days to RTP, is conditioned by the made available by the authors, without undue reservation. severity of the injury (Pedret et al., 2015; Balius et al., 2018, Balius et al., 2020) and by the myoconnective junction involved. The days to RTP are strongly associated with changes in Xc ETHICS STATEMENT (muscular fibers retraction quantified by % different of Xc) i.e., the severity of injuries is reflected by higher changes in Ethics approval was obtained from the Medical Committee Xc and longer time to RTP. Injury recovery is related to a of Barça Innovation Hub in Futbol Club Barcelona according readjustment of the Xc parameter closer to the value of the to principles of the Helsinki Declaration for experiments Frontiers in Physiology | www.frontiersin.org 10 September 2020 | Volume 11 | Article 574124 Nescolarde et al. MCJ Injuries by L-BIA with human beings. The participants provided oral and FUNDING written informed consent before participation in the study during a period of 2016–2017 and 2017–2018. The This study was supported by the Electronic and Biomedical patients/participants provided their written informed consent Instrumentation Research Group of Electronic Engineering to participate in this study. Department, Universitat Politècnica de Catalunya and FCB Medical Department, Barcelona, Spain. AUTHOR CONTRIBUTIONS All authors designed the experiments, analyzed the data, revised ACKNOWLEDGMENTS the manuscript, and approved the final version of the manuscript. 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The use, distribution or reproduction in other forums is permitted, positioning for human and animal electrical impedance myography research. provided the original author(s) and the copyright owner(s) are credited and that the Sci. Rep. 6:32615. original publication in this journal is cited, in accordance with accepted academic Schneider-Kolsky, M. E., Hoving, J. L., Warren, P., and Connell, D. A. (2006). practice. No use, distribution or reproduction is permitted which does not comply A comparison between clinical assessment and magnetic resonance imaging with these terms. Frontiers in Physiology | www.frontiersin.org 12 September 2020 | Volume 11 | Article 574124