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article 2019 21 pages

Clinical utility of tensiomyography for muscle function analysis in athletes

Oscar García-García, Alba Cuba-Dorado, Tania Álvarez-Yates, Javier Carballo-López, Mario Iglesias-Caamaño

Journal
Open Access Journal of Sports Medicine
DOI
10.2147/OAJSM.S161485
Publication type
Review Paper
Population
elite athletes
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Abstract

haustive review has been made tofilter the studies that have analyzed muscle function though tensiomyography (TMG) with elite or well-trained athletes. The results of this review indicate that the several protocols used in athletes tofind the displace- ment-time curve with greater maximum radial muscle displacement showed a good-excellent reliability. TMG has been used to characterize athletes’muscles contractile properties from specific sports disciplines, although there are very few sports that have been deeply analyzed. TMG seems to be useful to determine changes in muscles contractile properties after stimuli of competition, training or recovery. These changes have been strongly related with the fatigue produced after an effort. In addition, TMG parameters could be used to control training effects during a specific period or throughout the season being also a very useful tool to individualize athletes training loads. In this sense, it also seems to provide sports performance information in cyclic sports by relating some TMG parameters with perfor- mance indicators. On the other hand, the TMG-BCM algorithm has been used as a lateral and functional symmetry measure and as a monitoring tool for injury prevention and recovery. However, it seems to be no clear criterion that determines asymmetry degree, nor established contractile properties values as a reference to prevent or recover sports injuries. Despite the utility shown in thesefields, there are still very few sports analyzed and it is really necessary to continue advancing in the knowledge of the contractile properties behavior, such as the effects of athletes’training, competitions and injuries and even in the parameters interpreta- tion obtained with the TMG. Keywords:TMG, contractile properties, elite athletes, neuromuscular parameters, muscle assessment, muscle response Introduction Tensiomyography (TMG) has been used since the 1990s to evaluate the contractile properties of superficial muscles. It is a non-invasive method

the knowledge of the contractile properties behavior, such as the effects of athletes’training, competitions and injuries and even in the parameters interpreta- tion obtained with the TMG. Keywords:TMG, contractile properties, elite athletes, neuromuscular parameters, muscle assessment, muscle response Introduction Tensiomyography (TMG) has been used since the 1990s to evaluate the contractile properties of superficial muscles. It is a non-invasive method and does not require physical effort from the athlete. From our knowledge, the works of Burger et al 1 and Valencic and Knez 2 are the ones which show for thefirst time the possibility of obtaining a displacement-time curve of the superficial skeletal muscle through a displacement sensor with a certain pretension on the muscle belly. Later, this type of sensor would be validated as a micromachined accelerometer for muscle belly radial displacement measurement. 3 Currently, this type of displacement sensor (contact sensor) has been compared with a laser sensor (without contact with the muscular belly): both sensors obtained good to excellent test–retest reliability, as well as similar displacement and time measurements. 4 Though, the sensors showed Correspondence: Oscar García-García Faculty of Education and Sport Sciences, University of Vigo, Campus A Xunqueira s/n. Pontevedra, Pontevedra 36005, Spain Tel +3 498 680 1772 Fax +3 498 680 1701 Email oscargarcia@uvigo.es Open Access Journal of Sports Medicine Dovepress open access to scientific and medical research Open Access Full Text Article submit your manuscript| www.dovepress.com Open Access Journal of Sports Medicine 2019:10 49–69 49 DovePress © 2019 García-García et al. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/ terms.php and incorporate the Creative Commons Attribution–Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php). http://doi.org/10.2147/OAJSM.S161485Open Access Journal of Sports Medicine downloaded from https://www.dovepress.com/ For personal use only.

uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php). http://doi.org/10.2147/OAJSM.S161485Open Access Journal of Sports Medicine downloaded from https://www.dovepress.com/ For personal use only.

some differences between them, although according to these authors, these differences could be clinically irrelevant. The TMG measures the radial deformation of the muscular belly produced by a single electrical stimulus of the musclefiber, whose duration can be 0.2, 0.5 or the traditionally used of a 1 ms. The intensity of the electrical stimulus can be modulated between 1 and 110 mA. As a result of this electrical stimulus, a displacement-time curve is recorded where the following parameters are integrated. Maximum radial muscle displacement (Dm) as the peak space transverse deformation in the muscle in mm. Contraction time (Tc) as the time in ms from 10% to 90% of Dm on the ascending curve. Delay time (Td) as the time in ms from onset to 10% of Dm on the ascending curve. Sustain time (Ts) as the time in ms between 50% of Dm on both the ascending and descending sides of the curve. Half-time relaxation (Tr) as the time taken from 90% to 50% of Dm on descending curve. In addition, several measures have been established derived from the relationship between the Dm and the Tc that could be called radial displacement velocity, normalized response velocity or velocity of deformation (V r,Vc,Vrn,V90,V10 or Vd), ie, as the rate (mm·s −1 ) between the peak radial displacement occurring during the time period of Tc (Dm80) and Tc [Dm80/Tc]. Still, more research is needed to establish the most appropriate way to standardize this derived measure. 5 To date, several reviews have been published about the use, utility, validity and reliability of this tool. However, it seems that part of these variables may be modulated by the evaluated population. In this line, the construct validity and reliability of TMG has been established, however not for specialist populations (ie, elite athletes), 5 so it seems appropriate to review the usefulness of the data provided by TMG for the development of well-trained and elite athletes. Therefore, the objective of this work is to deter- mine the usefulness of the TMG to analyze muscle func- tion in athletes. Literature search Between the months of May

however not for specialist populations (ie, elite athletes), 5 so it seems appropriate to review the usefulness of the data provided by TMG for the development of well-trained and elite athletes. Therefore, the objective of this work is to deter- mine the usefulness of the TMG to analyze muscle func- tion in athletes. Literature search Between the months of May and October of 2018, the search of relevant literature for this study was carried out. We searched the Scopus, Web of Science and Sport Discus databases using the following terms: (tensiomyo- graph* or TMG or tensiomiography) and (performance or sport or competiti*). This search produced more than 1,000 articles that were analyzed to select only articles related to the usefulness of Tensiomiography in well- trained athletes of different sports. Articles written in Spanish, English and Portuguese were taken into account. Figure 1 shows the search process and articles selection. Measurement protocols and reliability in athletes It is not the aim of this review to discuss the validity of the TMG since TMG would still require much more research dedicated to this topic before it could be considered a valid and reliable assessment tool. 6 Yet, it does seem necessary to analyze the TMG measurement protocols that have been used to evaluate the athletes' muscular function and the reliability they have shown. More and more authors 7–9 explicitly state the condition that the evaluator should be an expert, which requires that he has made a good number of measurements and its intra- evaluator reliability is very high. There is consensus that the protocol used aims tofind the displacement-time curve that has the highest Dm in the muscle. However, few studies specify which of the displa- cement-time curves are selected to extract the data from the TMG parameters. Wiewelhove et al 10 and Simola et al 11 specify that“average of two maximal twitches was used for futher analyzes”or Giovanelli et al 12 suggest recording two maximum responses for the subsequent analysis. Nevertheless, García-García et al 13 propose“only the curve with the highest maximum radial displacement was included in the analysis for each

the data from the TMG parameters. Wiewelhove et al 10 and Simola et al 11 specify that“average of two maximal twitches was used for futher analyzes”or Giovanelli et al 12 suggest recording two maximum responses for the subsequent analysis. Nevertheless, García-García et al 13 propose“only the curve with the highest maximum radial displacement was included in the analysis for each muscle assessed”.We suggest that the protocol with TMG must specify exactly Initial database search: Articles selected based on title: Articles selected based on abstract or subjects: Articles included in the review: 84 studies excluded based on abstract or subjects 4 studies excluded: 58 studies 62 studies 146 studies • Scopus: 1042 Web of Science: 236 Sport Discus: 329 2 with insufficient data 2 irrelevant information Figure 1Flowchart of the literature search and the selection process. García-García et al Dovepress submit your manuscript| www.dovepress.com DovePress Open Access Journal of Sports Medicine 2019:1050Powered by TCPDF (www.tcpdf.org)

which displacement-time curves are taken into considera- tion for the subsequent analysis. The most commonly protocols used with athletes are detailed in Table 1 The incremental protocol until reaching the“plateau”, has also been defined as until no future displacement of the muscle belly could be produced 9 or until the maximum displacement of the muscle belly was reached. 20–22 The incremental protocol until reaching the maximum stimulus, in our opinion, is the only one that allows deter- mining the maximal radial displacement of the muscle belly. In this sense, it is suggested that elite athletes usually reach the maximum Dm between 90 and 110 mA, while other non-athletic or recreational populations reach it at clearly lower intensities, so using other proto- cols with a limited number of stimuli does not seem the right solution with elite or well-trained athletes to obtain the maximum Dm. 5,13 The relative and absolute reliability of the TMG para- meters has been generally analyzed with non-healthy ath- letes, obtaining good results. 28 The results that reported the reliability of TMG parameters with athlete population also indicate a high reliability, generally measured through the intraclass correlation and to a lesser extent, through the coefficient of variation. The muscles usually evaluated were those of the lower limb (ie, biceps femoris, rectus femoris, vastus medialis (VM), etc.), although some stu- dies have also evaluated the upper limb (ie, trapezius, deltoideus, etc.). The use of different protocols does not seem to affect the TMG assessment reliability. Although it seems that the incre- mental protocol until the maximum stimulus has slightly higher values than the other two protocols (Table 1). As can be seen in Table 1, the incremental protocol up to the maximum stimulus has shown high reliability in Tc and Dm in professional cyclists, in elite kayakers men and women and in professional footballers. In the same way, the incre- mental protocol until reaching the“plateau”has shown a high reliability for Dm and Tc in team sports players and in combat sports athletes. A high reliability is also obtained with the single or some stimulus to concrete intensities in

Tc and Dm in professional cyclists, in elite kayakers men and women and in professional footballers. In the same way, the incre- mental protocol until reaching the“plateau”has shown a high reliability for Dm and Tc in team sports players and in combat sports athletes. A high reliability is also obtained with the single or some stimulus to concrete intensities in soccer players. Athletes´ stimulus response TMG has been used to measure the muscle response to different stimuli. Several works have focused their study Table 1TMG protocols used in scientific literature Protocol Description Study (year) ICC Sample Incremental until reaching maximum stimulus It starts with an intensity of 20–30 mA and increases progressively in 10 mA or in 5 mA until reaching the maximal sti- mulator output (110 mA). García-García et al 7 0.98 b –0.97 a Professional soccer players García-García et al 9 0.97 b –0.99 a García-García 15 - Professional cyclists García-García et al 16 - García-García et al 17 0.92 b –0.97 a García-García et al 13 0.97–0.99 García-García et al 18 0.94–0.96 Elite kayakers Incremental until reaching“plateau” It starts with an intensity of 20 mA- 30 mA and increases progressively, generally in 10 mA until the Dm suffers a descent or aflattening of the curve called “plateau” Alvarez-Diaz et al 19 - Soccer players Loturco et al 20 - Professional soccer players Gil et al 21 - Loturco et al 22 - Elite athletes c Giovanelli et al 12 - Mountain marathon runners de Paula Simola et al 11 - Cyclists strength athletes Wiewelhove et al 10 0.92–0.95 a 0.91–0.94 b Elite Juniors tennis players A single or some stimulis at specific intensities A single concrete intensity stimulus is applied and a only displacement-time curve is obtained Rey et al 23 - Soccer players Rey et al 24 - Rey et al 8 0.86 b –0.95 a García-Manso et al 25 - Ultraendurance triathletes Rodríguez-Ruiz et al 26 - Elite volleyball players Rodríguez-Ruiz et al 27 - Notes: a Dm; b Tc; c jumper, runners, throwers. Abbreviation:ICC: Intraclass correlation coefficient. Confidence Interval 95%. Dovepress García-García et al

Rey et al 23 - Soccer players Rey et al 24 - Rey et al 8 0.86 b –0.95 a García-Manso et al 25 - Ultraendurance triathletes Rodríguez-Ruiz et al 26 - Elite volleyball players Rodríguez-Ruiz et al 27 - Notes: a Dm; b Tc; c jumper, runners, throwers. Abbreviation:ICC: Intraclass correlation coefficient. Confidence Interval 95%. Dovepress García-García et al Open Access Journal of Sports Medicine 2019:10 submit your manuscript| www.dovepress.com DovePress 51Powered by TCPDF (www.tcpdf.org)

on the competition stimuli effect. After running a marathon or a mountain race the parameters related to time (Vc, Tc, Ts, Tr, Td) decrease while the radial muscle belly displacement (Dm) increases. This means a reduction of muscular stiffness and an increase of neuromuscular fatigue. 12,25,29,30 Very similar results are obtained with surfers after a bodyboard competition. 30 Thesefindings suggest that mountain runners could improve their perfor- mance through strength training 12 as well as ironman athletes (Table 2). 25 On the other hand, recovery stimuli effects on muscle properties have been evaluated (Table 2). A cold water immersion protocol (4x4 min at 4 ºC) in lower limbs of semi- professional players entails a decrease in Dm and an increase in response and contraction speed. 31 Though, no differences in contractile properties between elite soccer players who have worn or not a kinesiotape bandage for 3 days. 32 Regarding the sports practice stimuli, a tumbling session produces a reduction in Tc and in Td of gymnasts’biceps femoris (BF), without affecting the same way to the rectus femoris (RF). 33,34 Also in relation with gymnasts, an increase in Vr, Ts and a decrease in Dm (increase in stiff- ness) and Tr was determined in the BF of young gymnasts after performing a muscle stretching session through static- stretching and contract-relax. These changes were more marked with the contract-relax method (Table 2). 35 Concerning to resistance stimuli (Table 2), a 6-day running-based HIIT-microcycle with a total of 11 sessions provokes an increase in the Tc of RF and the BF on male and female team sport athletes without any differences in the Dm. 36 However, there are no changes in junior tennis players after a 4-day HIIT microcycle, despite having significantly (p<0.001) reduced performance. 10 The effect of strength training stimuli during a short period of time has also been evaluated with TMG. 37 The results suggest that TMG can detect fatigue caused by high-resistance strength training in combat sports and intermittent game sports, since muscle contractile properties (ie, Dm, Vc) are reduced in the same way as performance indicators (ie, 1RM,

reduced performance. 10 The effect of strength training stimuli during a short period of time has also been evaluated with TMG. 37 The results suggest that TMG can detect fatigue caused by high-resistance strength training in combat sports and intermittent game sports, since muscle contractile properties (ie, Dm, Vc) are reduced in the same way as performance indicators (ie, 1RM, CMJ, etc.). In this sense, it has also been reported that the changes in Dm, Tc and Vc after a 6-day intensified strength training microcycle distinguishes between athletes trained in strength or endurance, and ensure regular mon- itoring of athletes´ fatigue and recovery status. The sports practice surface has also been used as exter- nal stimuli to evaluate its influence on the contractile prop- erties measured through TMG. Specifically, the RF and BF have been evaluated performing tests over different sports surfaces. 38,39 In female amateur rugby players the Tc and Dm values in RF after performing a repeated-sprint ability shuttle test on sand and natural grass were higher in sand than in natural grass, while in BF no significant differences were found between both surfaces (Table 2). 38 However, no significant differences were found in amateur soccer players neuromuscular responses between artificial turf and natural grass after completing three bouts of soccer simulation protocol on each surface. 39 On the other hand, the changes in muscle mechanics in vastus lateralis (VL), RF, VM, BF and gastrocnemius medialis (GM) after a training protocol in three different elastic platforms (gymnasticsfloor, tum- bling track and trampolining) showed that the trampolining fatigue levels and recovery time were higher in VM and BF than in gymnasticsfloor and tumbling . 40 In summary, the TMG seems to be useful to determine muscle contractile properties changes after competition, training and recovery stimulus. These changes can be related to muscle fatigue which would help to decide the athlete’s next training load orientation. In addition, TMG can also be useful to check the surface muscle fatigue influence in which the sports activity is carried out, obser- ving that softer surfaces affect fatigue and recovery time in a greater

after competition, training and recovery stimulus. These changes can be related to muscle fatigue which would help to decide the athlete’s next training load orientation. In addition, TMG can also be useful to check the surface muscle fatigue influence in which the sports activity is carried out, obser- ving that softer surfaces affect fatigue and recovery time in a greater extent after exertion, while it seems that sports practice on artificial turf does not cause greater fatigue than natural grass. Training period and/or competition effect TMG has also been used to measure muscle contractile properties changes during training periods. The purpose of these measurements has been to determine the effect of certain training loads and competitions during a mesocycle or the season. If a mesocycle is taken as reference (training period where an objective of acute training effect has been reached), the soccer players have been the athletes who have received the most attention (Table 2). A 6-week iso- metric-concentric strength training mesocycle produces a decrease in Tc and an increase in Dm in the RF of young soccer players, whereas if it is only a concentric strength training mesocycle produces the opposite effect. 46 Professional soccer players also seem to have changes of muscles contractile properties with trainings and competi- tions. For example, they decrease their Vc in the BF and RF muscles together with a decrease in their sprint speed, both linear and with change of direction, after performing an 8-week endurance and strength-power training period, García-García et al Dovepress submit your manuscript| www.dovepress.com DovePress Open Access Journal of Sports Medicine 2019:1052Powered by TCPDF (www.tcpdf.org)

Description

This review evaluates the utility of TMG in analyzing muscle function in athletes.