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The analyses of their age-group differences, sexual dimorphism, asymmetry characteristics in body regions, in sports having different pattern of physical loading could serve important information in this topic. 175 elite Hungarian handball players aged between 14 and 21 years were examined in 2023. Muscle mass component of the body segments was estimated by DEXA method and muscle thickness of the anterior mid-thigh region was measured by a new ultrasonic technique. The strength of knee extensor muscles was assessed by using an isokinetic protocol (Kineosystem dynamometer). A strong association between muscle robusticity and strength in the thigh region was confirmed in males, but not in females. Asymmetry in muscle mass reflected in the asymmetry in the knee extensor strength. A new predictive equation of muscle mass in the jumping leg and the total body from the muscle thickness in the anterior mid-thigh region of jumping leg was introduced. The exploration and understanding of asymmetric structural and functional adaptations can help athletes and trainers in planning the training and training interventions to reduce the risk of injuries. young athletes handball players inter-limb asymmetry strength and robusticity of the thigh Figures Figure 1 Figure 2 Figure 3 Introduction Research of the past decades revealed how training adaptations sum up as the changes of the structural and functional parameters of athletes’ muscles. Obviously, the differences in the pattern of activity loading and training modalities are reflected differently in the morphological and compositional indices of the underlying tissues, the muscular strength and performance, as well as the health and fitness parameters of athletes [ 1 – 3 ]. However, the relationship between morphological, compositional parameters of the human body and the strength indices, injury risk in young athletes has not fully been explored. The deeper understanding of the complex relationship among the training-related changes of structural and functional parameters in athletes could help to increase their functional performance level, fitness and health and to decrease the risk of injuries and overloading. Among other potential factors, asymmetry in muscular development is one of the main factors that influence skeletal muscle performance characteristics. Asymmetric sports can lead to asymmetric distribution of muscle mass, tonus and strength, and this may lead to irregularities, asymmetry in the skeletal structure [ 4 ]. These skeleto-muscular asymmetries may result in joint overloading, pain, injuries and degenerative changes, too [ 5 ]. The exploration and understanding of asymmetric structural and functional adaptations can help athletes and trainers in planning the training and training interventions to reduce the risk of injuries [ 6 – 7 ]. Handball is among the sports that expose the body to unilateral loading, particularly in throwing and jumping [ 8 – 9 ]. The former research results on the inter-limb asymmetries in physical performance of handball players revealed that (1) performance outcome of the throwing arm and jumping leg was, not surprisingly, better in handball players in tests connected with throwing or jumping performance; (2) tests of running performance or change of direction speed indicated a 10% limit of inter-limb asymmetry, inter-limb asymmetry larger than 10% was associated with reduced risk of injuries [e.g. 10–11]. However, it is emphasized by the differences of the former research results, that a single threshold of inter-limb asymmetry may not be used to predict the risk of lower performance or an injury. Sports- and test-specific, age- or maturation status-related thresholds are required to evaluate the asymmetry profile of athletes. The main purposes of the analysis were (1) to study the morphological and strength parameters of the thigh region in elite handball players to explore age-group differences, sexual dimorphism, asymmetry characteristics of the structural and functional parameters in the studied body region and the associations among the studied parameters, and (3) to establish regression equations for the estimation of muscle mass from muscle thickness and anthropometric measures. Subjects and Methods Participants Altogether 116 male and 57 female elite handball players, aged between 13.6 and 21.2 years (Table 1 ) were examined between March and June 2023 in the Sport Sciences and Diagnostic Research Centre of the Hungarian Handball Federation. Handball players were members of the respective age-group national team (U17, U19, and U21) or were selected through a talent selection program for the U15 age-group. The research protocol and procedures used were reviewed and approved by the Committee of the Hungarian Handball Federation in 2023. Written informed consent was obtained from the legal guardians of children and also from the study participants as well, and assent was obtained from the children as well. The examinations were carried out following the rules of the Declaration of Helsinki of 1975, revised in 2013. Table 1 The distribution of the sample by sex and age in the studied national handball teams, and the age-group means (± SD) of body mass and body height Males Females Teams n Age (years) Body mass (kg) Body height (cm) n Age (years) Body mass (kg) Body height (cm) U15 64 14.9 ± 0.5 69.9 ± 10.6 180.9 ± 6.2 20 14.9 ± 0.5 65.3 ± 10.5 171.5 ± 6.2 U17 12 16.5 ± 0.5 82.2 ± 12.1 187.8 ± 4.8 19 16.4 ± 0.6 65.8 ± 9.2 170.8 ± 6.3 U19 18 18.7 ± 0.6 88.0 ± 7.0 191.0 ± 5.9 18 18.7 ± 0.3 68.5 ± 9.4 174.0 ± 7.3 U21 22 20.6 ± 0.6 92.7 ± 12.4 192.2 ± 6.4 - - - - Together 116 57 Outcome measures Body structural examinations Quadriceps musculature thickness estimation. The thickness of the quadriceps muscle components (rectus femoris and vastus intermedius) in the anterior middle compartment of the thigh was measured by ultrasonography (BodyMetrix BX-2000, IntelaMetrix Inc., CA, USA) with an A-mode ultrasound imaging unit. Measurements were taken at the middle of the distance between the lateral condyle of the femur and the greater trochanter in sitting position with the hip and knee flexed at 90°. The sum of the thicknesses of rectus femoris and vastus intermedius was used to estimate the musculature thickness in the anterior mid-thigh region on both sides of the body. DEXA examinations. Body mass components (muscle, bone, and fat mass, both total and regional components) were measured with a GE Lunar Prodigy dual-energy X-ray scanner (GE Healthcare, Madison, WI, USA). Isokinetic knee extension dynamometry Strength testing of the knee extensor muscles was performed on a Kineosystem dynamometer (Domino s.r.l, Cordogne, Italy) using an isokinetic protocol at 60°/s angular velocity. The athletes were seated upright using straps to stabilize their trunk, hip, and thigh. Knee rotation axis was aligned to the lateral condyle. The athletes were allowed to grab chair handlings. A warmup protocol was performed prior to testing, which included five leg extensions with both legs and 3–3 unilateral leg extensions with the left and right leg with no external resistance. The testing protocol included three maximal extensions on the left and then on the right leg at 60°/s angular velocity with 30 s rest between repetitions. Verbal encouragement for maximal effort was provided throughout testing. Peak and average torque was calculated and used in statistical analysis. Data collection on injuries Data on the injuries of the lower extremities in the 12 months were collected by a self-administered questionnaire. Injuries not because of sporting activities were excluded from the analysis. Statistical analyses Centile curves of the studied muscular robusticity and strength indices were constructed by LMS method (LMS chartmaker pro version 2.3). As the central tendency of the indices the median centile was presented in the figures with the individual raw data. To study the relationship between the indices of muscular robusticity Pearson correlations of the indices were estimated and linear regression analysis was performed. Correlation coefficients higher than 0.5 were considered as strong correlations [ 12 ]. The prediction equations for DEXA muscle masses were developed by using a double cross-validation technique. Players were split into two subgroups of ‘odd’ and ‘even’ based on their age in both sexes (odd youngest, even second youngest, etc. so the two subgroups in males and females did not differ in terms of age). The regression equations (for jumping leg and total body muscle mass) were developed for the subgroups in both sexes, with the opposite group being used to cross-validate the equations. Since the equations were similar (evaluated by a comparison of R 2 values, errors of estimates and Bland-Altman graphs – graphs are not presented, the standardized residuals in all the subgroups in both sexes both in the case of lower extremity and total muscle mass estimates with the exception of 2 females’ total muscle mass and 3 females in the case of jumping leg muscle mass) the subgroups were combined and single equations were developed using the entire groups of males and females. Results Muscle robusticity and strength by age The muscle mass in the lower extremity and the muscle thickness of the anterior mid-thigh region (sum of the thickness of rectus femoris and vastus intermedius muscles, Fig. 1 ) of the jumping leg side showed very similar pattern by age in both sexes. Both studied muscular robusticity indices increased until the age of 16 in male athletes, then showed an interim plateau until the age of 20. After 20 years of age the muscular robusticity of the lower extremity in males showed an increase until the end of the studied age interval. The developmental pattern in the knee extensors strength of the jumping leg was very similar to that of muscular robusticity (muscle mass and thickness) in males (Fig. 1 a). The growth pattern of muscle mass and thickness in the lower extremity was less intense in the case of female athletes than in males (Fig. 1 b). In the studied age interval, muscle morphology did not show an acceleration after puberty, exception for muscle thickness in the anterior mid-thigh region: a slight increase could be observed until the age of 18 in females. Although the muscular thickness of the thigh region showed a slight increase by age in females in the studied age interval, knee extensors strength did not increase by age, female handball players tended to reach their maximal extension strength in the beginning of the studied age interval (Fig. 1 b). Morphological and functional asymmetry in the thigh region of the lower extremities The inter-limb asymmetry (its absolute amount and its variability) in muscle robusticity was smaller both in males and females than in the knee extensors strength (Fig. 2 ). The asymmetry in the studied structural and functional indicators of the thigh region did not revealed changes by age with the exception of the muscle thickness in males (Pearson correlation, r: 0.258, p < 0.05), a shift toward the thicker thickness of musculus quadriceps in the dominant leg was observed by age in males in the studied age interval. The association between the muscular robusticity and strength of the thigh region The strength of the knee extensors showed strong correlation with the muscle mass of the leg and strong or moderate correlation with the muscle thickness of the anterior mid-thigh (Table 2 ) both in the jumping and the opposite legs in male handball players. In females the associations were much weaker between the studied morphological and strength parameters of the thigh, namely, moderate correlations were found between the muscle mass and strength of the thigh in both legs, and the association was not significant between the strength and muscle thickness of the anterior region of the thighs (Table 2 ). The bilateral asymmetry in the morphological and strength parameters of the legs revealed significant association only for peak torque (60°/s) in males and for the average and peak torque (60°/sec) in females, in the case of muscle mass asymmetry in both sexes (Table 2 ). Table 2 Pearson correlation coefficients between knee extensors and structural indices of the lower extremities (correlations were significant at the level of 0.05 in the case of the presented coefficients, ns: correlation was not significant) Jumping leg Opposite leg Leg strength Muscle mass (kg) Muscle thickness (mm) Muscle mass (kg) Muscle thickness (mm) Males Average, 60°/s 0.748 0.519 0.813 0.602 Peak, 60°/s 0.773 0.494 0.765 0.491 Females Average, 60°/s 0.600 ns 0.645 ns Peak, 60°/s 0.665 ns 0.652 0.321 Males (bilateral asymmetry) Females (bilateral asymmetry) Muscle mass (kg) Muscle thickness (mm) Muscle mass (kg) Muscle thickness (mm) Average, 60°/s ns ns 0.406 ns Peak, 60°/s 0.245 ns 0.317 ns Muscle mass estimation equation for the lower extremities Strong correlations were observed between the muscle mass and thickness parameters (Table 3 ) in the jumping leg. Our aim was to find the strongest DEXA muscle mass prediction equation for the lower extremities based on anthropometric and ultrasonic measurements. By regarding the relationships between muscle mass (total and regional) and thickness in the anterior mid-thigh region (Table 3 , Fig. 3 ), DEXA muscle mass could be estimated from muscle thickness and other muscular robustness predictors as well. Table 3 Pearson correlation coefficients of the relations between the studied muscular robusticity and strength indicators (p < 0.001 in both sexes and in all the studied relations) Muscle mass (total) Muscle mass (jumping leg) Muscle mass (opposite leg) Muscle thickness -AM thigh (jumping leg) Muscle thickness -AM thigh (opposite leg) Boys Muscle mass (total) Girls - 0.963 0.972 0.664 0.596 Muscle mass (jumping leg) 0.961 - 0.968 0.666 0.603 Muscle mass (opposite leg) 0.962 0.959 - 0.642 0.586 Muscle thickness -AM thigh (jumping leg) 0.404 0.371 0.414 - 0.806 Muscle thickness -AM thigh (jumping leg) 0.345 0.287 0.318 0.778 - The prediction of muscle mass in the jumping leg and in the whole body by using muscle thickness in the AM thigh, body mass and stature was significant in males, and revealed that more than 93% and 95%, resp. variability in muscle mass of the studied regions was accounted for these 3 predictors (Table 4 ). In female athletes only body mass and muscle thickness in the AM thigh region were enough to predict muscle mass in the jumping leg or total body muscle mass: more than 91% and 94%, resp. of variability in muscle mass in the studied body regions was accounted AM thigh muscle thickness and body mass (Tables 4 –5). Discussion The muscle mass, thickness and strength in the studied body region of male handball players revealed an increase in puberty, and young adult male players muscular robusticity and strength increased after 10 years of age. Contrary to males, muscular robusticity and strength in females did not change intensively by age in jumping leg, female handball players seemed to reach their muscular strength and robusticity until the age of 14–16. The strong association between muscle robusticity and strength in the thigh region was confirmed in males, and between muscle mass and strength in females, but not in muscle thickness in females in the studied group of young handball players. Asymmetry is beneficial in special sports, however, increased bilateral asymmetry (asymmetry in skeleto-muscular robusticity, strength etc.), or the discrepancy from the sport-dependent, typical skeleto-muscular asymmetry may increase the injury risk and may decrease the physical performance in athletes. Experts suggest compensatory exercises for athletes if a higher ratio of robusticity or strength asymmetry is discovered. Former studies revealed that a 10–15% muscle robusticity or strength asymmetry in athletes is considered as an indicator of significant muscular unbalance that is associated with a higher risk of injuries [e.g. 13]. This tendency could be confirmed and if the non-jumping leg showed a 5–10% overdevelopment compared to the jumping leg in male handball players. However, a protective effect of 5–10% muscular robusticity dominance in favour of the jumping leg appeared in both sexes in the studied group of handball players. A certain amount (5–10%) asymmetry in the muscular development of the lower extremities, the 5–10% overdevelopment of the jumping comparing to the non-jumping leg, seemed to decrease the risk of leg injuries in this type of sports, when the jumps are so important among the movements, when the jumps with hard landings, rapid changes of movement, frequent contacts and collisions between players characterise the game [ 14 ]. By considering the age differences in the structural and/or functional inter-limb asymmetry in young athletes, the results have been controversial: former studies revealed no differences or increasing asymmetry by age in the during the pubertal period around the onset of peak height velocity [ 11 , 15 – 17 ]. The present study confirmed that inter-limb asymmetry did not change by age in young handball players in the studied age interval. The higher level of asymmetry in the functional parameters compared to the structural ones in the thigh region of the lower extremity was found in both sexes in young athletes. This trend might be explained by that beside the development of the anatomical structures several factors influence the development of the functional capacities, as the learning of sports skills, the development of the nervous system etc. Injuries of the lower extremities were more frequent in female than in male athletes (19% in males, 29.6% in females) in the studied sample of young elite handball players. An 5–10% asymmetry in the muscular robusticity of the legs in favour of the jumping leg revealed protection against leg injuries in handball players (injury prevalence in the lower extremities by the asymmetry categories 10%: males – 18.2%, females – 27.3%, chi 2 test, p < 0.05 in both sexes). A new predictive equation of muscle mass in the jumping leg and the total body from the muscle thickness in the anterior mid-thigh region of jumping leg was introduce by analysing the relationship between DEXA muscle mass estimations and ultrasonic measures of quadriceps femoris in the thigh. The muscle mass estimation based on ultrasonography (BodyMetrix BX-2000) of muscle layers could be a reliable, accurate radiation-free, quick and easy alternative of DEXA estimation that can serve regularly information on muscle robusticity. We have already started the examinations of muscle robusticity in the upper extremities and in the trunk to construct muscle mass estimation equations also for these body regions in athletes that require only ultrasound measurements of muscle layers. Conclusion Muscular asymmetry, i.e. interlimb asymmetry in robusticity, strength, coordination and motor control between right and left extremities in athletes is considered a risk factor for an increased level of sports injuries. The analyses of asymmetry in the structural and functional indices of muscle development in handball players aged 14–20 were performed to serve information for a future screening method of inter-limb asymmetry profile of young athletes. Our further aim is to construct such a screening method by studying the relationship between muscle thickness, strength, injury prevalence in the mirror of the asymmetry profile of young athletes in the other body regions, too. Limitations Bilateral strength measured by isokinetic test and muscular robusticity in the same muscle group are sometimes not be verified by functional tests of the studied body region, since other muscle groups might compensate the developmental differences, asymmetries between the two sides of the given body region. Therefore, isokinetic tests should be identified by the kinetic tests (e.g. jumping on a force platform). Kinetic tests were also performed in the studied sample of athletes, however, the comparison of kinetic and isokinetic tests did not fit the topic of the present manuscript. Muscle mass was measured by DEXA for the whole lower extremity, not only for the thigh segment of the extremity. Although the correlation between the muscle mass in thigh region and the whole lower extremity is very high, this methodological limitation should be considered. The weak or missing association of the parameters of the unity of structure and extension strength in the anterior region of the thighs suggests that other effects (ration of the 2 types of muscle fibres, thigh and muscle length, tendon insertion morphology etc.) should be considered in the future analyses in the bigger sample of elite athletes. Furthermore, the level of fatigue and overtraining should be also considered in such analyses. Our aim is to increase the sample size and complete the analysis by collecting information on the above-mentioned variables in a subsample of athletes, and to develop a new method for the estimation of the level of overtraining by using endocrine-immune and physical performance predictors. Declarations Author Contributions AZs: research design, data collection, analysis, writing the article, conceptualization, supervision. FZsR-S: data collection, writing the article, conceptualization, visualization. CsJ-K: data collection, writing the article. LP: research design, data collection, analysis, writing the article, conceptualization, supervision. PB: research design, data collection, analysis, writing the article. IJ: analysis, writing the article, conceptualization. TSz: research design, data collection, analysis, writing the article, conceptualization, supervision. All authors have read and agreed to the submitted version of the manuscript. Funding This research received no external funding. Institutional Review Board Statement The study was reviewed and approved by the Committee of the Hungarian Handball Federation in 2023 (approval No: 1/2023, Budapest, January 2023) and by the Committee of the Doctoral School of Biology, Eotvos Lorand University, Budapest, Hungary in July 2022. Informed Consent Statement Written informed consent was obtained from the legal guardians of children, and assent was obtained from the children as well. Data Availability Statement The data presented in this study are available on request from the corresponding author (AZs). Conflicts of Interest The authors declare no conflicts of interest. References Friedmann-Bette, B., Bauer, T., Kinscherf, R., Vorwald, S., Klute, K., Bischoff, D., Müller, H., Weber, M.A., Metz, J., Kauczor, H.U., & Bärtsch, P. Effects of strength training with eccentric overload on muscle adaptation in male athletes. Eur. J. Appl. Physiol. 2010 , 108 , 821–836. https://doi.org/10.1007/s00421-009-1292-2 Legerlotz, K., Marzilger, R., Bohm, S., & Arampatzis, A. Physiological adaptations following resistance training in youth athletes—a narrative review. Pediatr. Exerc. Sci. 2016 , 28(4) , 501–520. https://doi.org/10.1123/pes.2016-0023 Mersmann, F., Bohm, S., Schroll, A., Boeth, H., & Duda, G.N., Arampatzis, A. Muscle and tendon adaptation in adolescent athletes: a longitudinal study. Scand. J. Med. Sci. Sports . 2017 , 27(1) , 75–82. https://doi.org/10.1111/sms.12631 Kadri, M.A., Noe, F., Maitre, J., Maffulli, N., & Paillard, T. Effects of limb dominance on postural balance in sportsmen practicing symmetric and asymmetric sports: A pilot study. Symmetry . 2021 , 13(11) , 2199. https://doi.org/10.3390/sym13112199 Hietamo, J., Parkkari, J., Leppanen, M., Steffen, K., Kannus, P., Vasankari, T., Heinonen, A., Mattila, V.M., & Pasanen, K. Association between lower extremity muscular strength and acute knee injuries in young team‐sport athletes. Transl. Sports Med. 2020 , 3(6) , 626–637. https://doi.org/10.1002/tsm2.172 Menzel, H.J., Chagas, M.H., Szmuchrowski, L.A., Araujo, S.R., de Andrade, A.G., & de Jesus-Moraleida, F.R. Analysis of lower limb asymmetries by isokinetic and vertical jump tests in soccer players. J. Strength Cond. Res. 2013 , 27(5) , 1370–1377. https://doi.org/10.1519/JSC.0b013e318265a3c8 Theodorou, E., Tryfonidis, M., & Zaras, N., Hadjicharalambous, M. Musculoskeletal Asymmetries in Young Soccer Players: 8 Weeks of an Applied Individual Corrective Exercise Intervention Program. Appl. Sci. 2023 , 13(11) , 6445. https://doi.org/10.3390/app13116445 Lijewski, M., Burdukiewicz, A., Pietraszewska, J., Andrzejewska, J., & Stachon, A. Asymmetry of Muscle Mass Distribution and Grip Strength in Professional Handball Players. Int. J. Environ. Res. Pub. Health. 2021 , 18(4) , 1913. https://doi.org/10.3390/ijerph18041913 Madruga-Parera, M., Bishop, C., Beato, M., Fort-Vanmeerhaeghe, A., Gonzalo-Skok, O., & Romero-Rodriguez, D. Relationship between interlimb asymmetries and speed and change of direction speed in youth handball players. J. Strength Condit. Res. 2021 , 35(12) , 3482–3490. https://doi.org/10.1519/JSC.0000000000003328 Bishop, C. Inter-limb Asymmetries: Are Thresholds a Usable Concept? Strength Condit. J. 2021 , 43(1) , 32–36. https://doi.org/10.1519/0000000000000554 Cadens, M., Planas-Anzano, A., Peirau-Terés, X., Bishop, C., Romero-Rodríguez, D., & Madruga-Parera, M. Relationship between Asymmetry Profiles and Jump Performance in Youth Female Handball Players. J. Hum. Kin. 2023 , 88 , 5–16. https://doi.org/10.5114/jhk/163432 Koo, T.K., Li, & M.Y. 2016. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J. Chiropract. Med. 2016 , 15(2) , 155–163. https://doi.org/10.1016/j.jcm.2016.02.012 Asai, K., Nakase, J., Shimozaki, K., Toyooka, K., Kitaoka, K., & Tsuchiya, H. Incidence of injury in young handball players during national competition: A 6-year survey. J. Orthopaed. Sci. 2020 , 25(4) , 677–681. https://doi.org/10.1016/j.jos.2019.06.011 Vargas, V.Z., Motta, C., Peres, B., Vancini, R.L., De Lira, C.A.B., & Andrade, M.S. Knee isokinetic muscle strength and balance ratio in female soccer players of different age groups: A cross-sectional study. Phys. Sportsmed. 2019 , 48 , 105–109. https://doi.org/10.1080/00913847.2019.1642808 Read, P., Oliver, J., Myer, G., De Ste Croix, M., & Lloyd, R. (2017). The Effects of Maturation on Measures of Asymmetry During Neuromuscular Control Tests in Elite Male Youth Soccer Players. Pediatr. Exerc. Sci. 2017 , 30(1) , 168–175. https://doi.org/10.1123/pes.2017-0081 Madruga-Parera, M., Romero-Rodriguez, D., Bishop, C., Beltran-Valls, M. R., Latinjak, A. T., Beato, M., & Fort-Vanmeerhaeghe, A. Effects of Maturation on Lower Limb Neuromuscular Asymmetries in Elite Youth Tennis Players. Sports . 2019 , 7(5) , 106. https://doi.org/10.3390/sports7050106 Pardos-Mainer, E., Bishop, C., Gonzalo-Skok, O., Nobari, H., Pérez-Gomez, J., & Lozano, D. Associations between inter-limb asymmetries in jump and change of direction speed tests and physical performance in adolescent female soccer players. Int. J. Environ. Res. Public Health. 2021 , 18(7) , 3474. https://doi.org/10.3390/ijerph18073474 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 21 Nov, 2024 Read the published version in Scientific Reports → Version 1 posted Reviews received at journal 18 Aug, 2024 Reviews received at journal 09 Aug, 2024 Reviewers agreed at journal 05 Aug, 2024 Reviewers agreed at journal 05 Aug, 2024 Reviewers invited by journal 05 Aug, 2024 Editor assigned by journal 04 Aug, 2024 Editor invited by journal 23 Jul, 2024 Submission checks completed at journal 22 Jul, 2024 First submitted to journal 15 Jul, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4743772","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":340540935,"identity":"ffa8dd93-2863-4e84-bcfe-e7de1bf1999f","order_by":0,"name":"Annamaria 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ELTE","correspondingAuthor":false,"prefix":"","firstName":"Fanny","middleName":"Zselyke","lastName":"Ratz-Sulyok","suffix":""},{"id":340540937,"identity":"19753894-4d49-4277-b84c-6eb412fa1e18","order_by":2,"name":"Csilla Jang-Kapuy","email":"","orcid":"","institution":"Eotvos Lorand University, ELTE","correspondingAuthor":false,"prefix":"","firstName":"Csilla","middleName":"","lastName":"Jang-Kapuy","suffix":""},{"id":340540938,"identity":"6a492135-d514-41a5-a37b-4f6fbd68e7f0","order_by":3,"name":"Leonidas Petridis","email":"","orcid":"","institution":"Hungarian University of Sport Sciences","correspondingAuthor":false,"prefix":"","firstName":"Leonidas","middleName":"","lastName":"Petridis","suffix":""},{"id":340540939,"identity":"fb810de8-e452-4fbc-ad09-d4bbed020203","order_by":4,"name":"Peter Bakonyi","email":"","orcid":"","institution":"Hungarian Handball Federation","correspondingAuthor":false,"prefix":"","firstName":"Peter","middleName":"","lastName":"Bakonyi","suffix":""},{"id":340540940,"identity":"bf87faf9-7de9-4329-913e-8827a4098016","order_by":5,"name":"Istvan Juhasz","email":"","orcid":"","institution":"Hungarian Handball Federation","correspondingAuthor":false,"prefix":"","firstName":"Istvan","middleName":"","lastName":"Juhasz","suffix":""},{"id":340540941,"identity":"222629bc-6543-44ea-bb44-d3982a77dd79","order_by":6,"name":"Tamas Szabo","email":"","orcid":"","institution":"Hungarian Handball Federation","correspondingAuthor":false,"prefix":"","firstName":"Tamas","middleName":"","lastName":"Szabo","suffix":""}],"badges":[],"createdAt":"2024-07-15 15:03:46","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4743772/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4743772/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1038/s41598-024-75472-4","type":"published","date":"2024-11-21T15:56:54+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":62611718,"identity":"e898719d-cfd7-47f6-86e4-a86687116664","added_by":"auto","created_at":"2024-08-16 12:14:24","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":641834,"visible":true,"origin":"","legend":"\u003cp\u003eMuscle robustness and extension strength (60°/sec) indicators in the lower extremity (jumping leg) by age in male (a) and female (b) athletes (muscle mass: DEXA estimation, muscle thickness: BodyMetrix estimation on the anterior mid-thigh region of the lower extremity, .....: median centile)\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-4743772/v1/41555dce90c811a7767aab2e.png"},{"id":62611705,"identity":"4325c39f-c1f8-452e-ba0a-0633054edcd4","added_by":"auto","created_at":"2024-08-16 12:14:22","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":728760,"visible":true,"origin":"","legend":"\u003cp\u003eRelative (expressed in the percentage of dominant leg value) difference between the dominant and non-dominant muscle robusticity and strength (60°/sec, av: average, p: peak strength) in the lower extremity in male (a) and female (b) handball players (.....: median centile)\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-4743772/v1/4783d6a2c336358e7a357b41.png"},{"id":62611706,"identity":"3dd06095-dda7-40ba-b3b3-df0a30b3c548","added_by":"auto","created_at":"2024-08-16 12:14:23","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":289965,"visible":true,"origin":"","legend":"\u003cp\u003eThe linear relationship between muscle mass and thickness (AM thigh region) in the jumping leg (males: R\u003csup\u003e2\u003c/sup\u003e=0.44, females: R\u003csup\u003e2\u003c/sup\u003e=0.21)\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-4743772/v1/c2a5299966b36404a5e4a124.png"},{"id":69834848,"identity":"84aacfa4-0bb0-46e7-bcdd-f3fc71c41b65","added_by":"auto","created_at":"2024-11-25 16:09:31","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2142822,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4743772/v1/fa42a071-89cd-4e64-80d8-2e757b614b17.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Muscular robusticity and strength in the lower extremities in elite handball players","fulltext":[{"header":"Introduction","content":"\u003cp\u003eResearch of the past decades revealed how training adaptations sum up as the changes of the structural and functional parameters of athletes\u0026rsquo; muscles. Obviously, the differences in the pattern of activity loading and training modalities are reflected differently in the morphological and compositional indices of the underlying tissues, the muscular strength and performance, as well as the health and fitness parameters of athletes [\u003cspan additionalcitationids=\"CR2\" citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]. However, the relationship between morphological, compositional parameters of the human body and the strength indices, injury risk in young athletes has not fully been explored. The deeper understanding of the complex relationship among the training-related changes of structural and functional parameters in athletes could help to increase their functional performance level, fitness and health and to decrease the risk of injuries and overloading. Among other potential factors, asymmetry in muscular development is one of the main factors that influence skeletal muscle performance characteristics. Asymmetric sports can lead to asymmetric distribution of muscle mass, tonus and strength, and this may lead to irregularities, asymmetry in the skeletal structure [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. These skeleto-muscular asymmetries may result in joint overloading, pain, injuries and degenerative changes, too [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. The exploration and understanding of asymmetric structural and functional adaptations can help athletes and trainers in planning the training and training interventions to reduce the risk of injuries [\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eHandball is among the sports that expose the body to unilateral loading, particularly in throwing and jumping [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. The former research results on the inter-limb asymmetries in physical performance of handball players revealed that (1) performance outcome of the throwing arm and jumping leg was, not surprisingly, better in handball players in tests connected with throwing or jumping performance; (2) tests of running performance or change of direction speed indicated a 10% limit of inter-limb asymmetry, inter-limb asymmetry larger than 10% was associated with reduced risk of injuries [e.g. 10\u0026ndash;11]. However, it is emphasized by the differences of the former research results, that a single threshold of inter-limb asymmetry may not be used to predict the risk of lower performance or an injury. Sports- and test-specific, age- or maturation status-related thresholds are required to evaluate the asymmetry profile of athletes.\u003c/p\u003e \u003cp\u003eThe main purposes of the analysis were (1) to study the morphological and strength parameters of the thigh region in elite handball players to explore age-group differences, sexual dimorphism, asymmetry characteristics of the structural and functional parameters in the studied body region and the associations among the studied parameters, and (3) to establish regression equations for the estimation of muscle mass from muscle thickness and anthropometric measures.\u003c/p\u003e"},{"header":"Subjects and Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eParticipants\u003c/h2\u003e \u003cp\u003eAltogether 116 male and 57 female elite handball players, aged between 13.6 and 21.2 years (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) were examined between March and June 2023 in the Sport Sciences and Diagnostic Research Centre of the Hungarian Handball Federation. Handball players were members of the respective age-group national team (U17, U19, and U21) or were selected through a talent selection program for the U15 age-group. The research protocol and procedures used were reviewed and approved by the Committee of the Hungarian Handball Federation in 2023. Written informed consent was obtained from the legal guardians of children and also from the study participants as well, and assent was obtained from the children as well. The examinations were carried out following the rules of the Declaration of Helsinki of 1975, revised in 2013.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eThe distribution of the sample by sex and age in the studied national handball teams, and the age-group means (\u0026plusmn;\u0026thinsp;SD) of body mass and body height\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"9\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c5\" namest=\"c2\"\u003e \u003cp\u003eMales\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c9\" namest=\"c6\"\u003e \u003cp\u003eFemales\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTeams\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003en\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eAge (years)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eBody mass (kg)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eBody height (cm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003en\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eAge (years)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003eBody mass (kg)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003eBody height (cm)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eU15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e64\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e14.9\u0026thinsp;\u0026plusmn;\u0026thinsp;0.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e69.9\u0026thinsp;\u0026plusmn;\u0026thinsp;10.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e180.9\u0026thinsp;\u0026plusmn;\u0026thinsp;6.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e20\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e14.9\u0026thinsp;\u0026plusmn;\u0026thinsp;0.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e65.3\u0026thinsp;\u0026plusmn;\u0026thinsp;10.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e171.5\u0026thinsp;\u0026plusmn;\u0026thinsp;6.2\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eU17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e16.5\u0026thinsp;\u0026plusmn;\u0026thinsp;0.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e82.2\u0026thinsp;\u0026plusmn;\u0026thinsp;12.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e187.8\u0026thinsp;\u0026plusmn;\u0026thinsp;4.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e16.4\u0026thinsp;\u0026plusmn;\u0026thinsp;0.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e65.8\u0026thinsp;\u0026plusmn;\u0026thinsp;9.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e170.8\u0026thinsp;\u0026plusmn;\u0026thinsp;6.3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eU19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e18.7\u0026thinsp;\u0026plusmn;\u0026thinsp;0.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e88.0\u0026thinsp;\u0026plusmn;\u0026thinsp;7.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e191.0\u0026thinsp;\u0026plusmn;\u0026thinsp;5.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e18.7\u0026thinsp;\u0026plusmn;\u0026thinsp;0.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e68.5\u0026thinsp;\u0026plusmn;\u0026thinsp;9.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e174.0\u0026thinsp;\u0026plusmn;\u0026thinsp;7.3\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eU21\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e20.6\u0026thinsp;\u0026plusmn;\u0026thinsp;0.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e92.7\u0026thinsp;\u0026plusmn;\u0026thinsp;12.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e192.2\u0026thinsp;\u0026plusmn;\u0026thinsp;6.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTogether\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e116\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e57\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eOutcome measures\u003c/h2\u003e \u003cdiv id=\"Sec5\" class=\"Section3\"\u003e \u003ch2\u003eBody structural examinations\u003c/h2\u003e \u003cp\u003e \u003cb\u003eQuadriceps musculature thickness estimation.\u003c/b\u003e The thickness of the quadriceps muscle components (rectus femoris and vastus intermedius) in the anterior middle compartment of the thigh was measured by ultrasonography (BodyMetrix BX-2000, IntelaMetrix Inc., CA, USA) with an A-mode ultrasound imaging unit. Measurements were taken at the middle of the distance between the lateral condyle of the femur and the greater trochanter in sitting position with the hip and knee flexed at 90\u0026deg;. The sum of the thicknesses of rectus femoris and vastus intermedius was used to estimate the musculature thickness in the anterior mid-thigh region on both sides of the body.\u003c/p\u003e \u003cp\u003e \u003cb\u003eDEXA examinations.\u003c/b\u003e Body mass components (muscle, bone, and fat mass, both total and regional components) were measured with a GE Lunar Prodigy dual-energy X-ray scanner (GE Healthcare, Madison, WI, USA).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section3\"\u003e \u003ch2\u003eIsokinetic knee extension dynamometry\u003c/h2\u003e \u003cp\u003eStrength testing of the knee extensor muscles was performed on a Kineosystem dynamometer (Domino s.r.l, Cordogne, Italy) using an isokinetic protocol at 60\u0026deg;/s angular velocity. The athletes were seated upright using straps to stabilize their trunk, hip, and thigh. Knee rotation axis was aligned to the lateral condyle. The athletes were allowed to grab chair handlings. A warmup protocol was performed prior to testing, which included five leg extensions with both legs and 3\u0026ndash;3 unilateral leg extensions with the left and right leg with no external resistance. The testing protocol included three maximal extensions on the left and then on the right leg at 60\u0026deg;/s angular velocity with 30 s rest between repetitions. Verbal encouragement for maximal effort was provided throughout testing. Peak and average torque was calculated and used in statistical analysis.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eData collection on injuries\u003c/h2\u003e \u003cp\u003eData on the injuries of the lower extremities in the 12 months were collected by a self-administered questionnaire. Injuries not because of sporting activities were excluded from the analysis.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analyses\u003c/h2\u003e \u003cp\u003eCentile curves of the studied muscular robusticity and strength indices were constructed by LMS method (LMS chartmaker pro version 2.3). As the central tendency of the indices the median centile was presented in the figures with the individual raw data. To study the relationship between the indices of muscular robusticity Pearson correlations of the indices were estimated and linear regression analysis was performed. Correlation coefficients higher than 0.5 were considered as strong correlations [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. The prediction equations for DEXA muscle masses were developed by using a double cross-validation technique. Players were split into two subgroups of \u0026lsquo;odd\u0026rsquo; and \u0026lsquo;even\u0026rsquo; based on their age in both sexes (odd youngest, even second youngest, etc. so the two subgroups in males and females did not differ in terms of age). The regression equations (for jumping leg and total body muscle mass) were developed for the subgroups in both sexes, with the opposite group being used to cross-validate the equations. Since the equations were similar (evaluated by a comparison of R\u003csup\u003e2\u003c/sup\u003e values, errors of estimates and Bland-Altman graphs \u0026ndash; graphs are not presented, the standardized residuals in all the subgroups in both sexes both in the case of lower extremity and total muscle mass estimates with the exception of 2 females\u0026rsquo; total muscle mass and 3 females in the case of jumping leg muscle mass) the subgroups were combined and single equations were developed using the entire groups of males and females.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec10\"\u003e\n \u003ch2\u003eMuscle robusticity and strength by age\u003c/h2\u003e\n \u003cp\u003eThe muscle mass in the lower extremity and the muscle thickness of the anterior mid-thigh region (sum of the thickness of rectus femoris and vastus intermedius muscles, Fig. \u003cspan\u003e1\u003c/span\u003e) of the jumping leg side showed very similar pattern by age in both sexes. Both studied muscular robusticity indices increased until the age of 16 in male athletes, then showed an interim plateau until the age of 20. After 20 years of age the muscular robusticity of the lower extremity in males showed an increase until the end of the studied age interval. The developmental pattern in the knee extensors strength of the jumping leg was very similar to that of muscular robusticity (muscle mass and thickness) in males (Fig. \u003cspan\u003e1\u003c/span\u003ea).\u003c/p\u003e\n \u003cp\u003eThe growth pattern of muscle mass and thickness in the lower extremity was less intense in the case of female athletes than in males (Fig. \u003cspan\u003e1\u003c/span\u003eb). In the studied age interval, muscle morphology did not show an acceleration after puberty, exception for muscle thickness in the anterior mid-thigh region: a slight increase could be observed until the age of 18 in females. Although the muscular thickness of the thigh region showed a slight increase by age in females in the studied age interval, knee extensors strength did not increase by age, female handball players tended to reach their maximal extension strength in the beginning of the studied age interval (Fig. \u003cspan\u003e1\u003c/span\u003eb).\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec11\"\u003e\n \u003ch2\u003eMorphological and functional asymmetry in the thigh region of the lower extremities\u003c/h2\u003e\n \u003cp\u003eThe inter-limb asymmetry (its absolute amount and its variability) in muscle robusticity was smaller both in males and females than in the knee extensors strength (Fig. \u003cspan\u003e2\u003c/span\u003e). The asymmetry in the studied structural and functional indicators of the thigh region did not revealed changes by age with the exception of the muscle thickness in males (Pearson correlation, r: 0.258, p\u0026thinsp;\u0026lt;\u0026thinsp;0.05), a shift toward the thicker thickness of musculus quadriceps in the dominant leg was observed by age in males in the studied age interval.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec12\"\u003e\n \u003ch2\u003eThe association between the muscular robusticity and strength of the thigh region\u003c/h2\u003e\n \u003cp\u003eThe strength of the knee extensors showed strong correlation with the muscle mass of the leg and strong or moderate correlation with the muscle thickness of the anterior mid-thigh (Table \u003cspan\u003e2\u003c/span\u003e) both in the jumping and the opposite legs in male handball players. In females the associations were much weaker between the studied morphological and strength parameters of the thigh, namely, moderate correlations were found between the muscle mass and strength of the thigh in both legs, and the association was not significant between the strength and muscle thickness of the anterior region of the thighs (Table \u003cspan\u003e2\u003c/span\u003e).\u003c/p\u003e\n \u003cp\u003eThe bilateral asymmetry in the morphological and strength parameters of the legs revealed significant association only for peak torque (60\u0026deg;/s) in males and for the average and peak torque (60\u0026deg;/sec) in females, in the case of muscle mass asymmetry in both sexes (Table \u003cspan\u003e2\u003c/span\u003e).\u003c/p\u003e\n \u003cdiv\u003e\n \u003ctable id=\"Tab2\" border=\"1\"\u003e\n \u003ccaption language=\"En\"\u003e\n \u003cdiv\u003eTable 2\u003c/div\u003e\n \u003cdiv\u003e\n \u003cp\u003ePearson correlation coefficients between knee extensors and structural indices of the lower extremities (correlations were significant at the level of 0.05 in the case of the presented coefficients, ns: correlation was not significant)\u003c/p\u003e\n \u003c/div\u003e\n \u003c/caption\u003e\n \u003ccolgroup cols=\"5\"\u003e\u003c/colgroup\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003cth align=\"left\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eJumping leg\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eOpposite leg\u003c/p\u003e\n \u003c/th\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eLeg strength\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle\u003c/p\u003e\n \u003cp\u003emass (kg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle thickness (mm)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle\u003c/p\u003e\n \u003cp\u003emass (kg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle thickness (mm)\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"4\"\u003e\n \u003cp\u003eMales\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eAverage, 60\u0026deg;/s\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.748\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.519\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.813\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.602\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ePeak, 60\u0026deg;/s\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.773\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.494\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.765\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.491\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"4\"\u003e\n \u003cp\u003eFemales\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eAverage, 60\u0026deg;/s\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.600\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.645\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ePeak, 60\u0026deg;/s\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.665\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.652\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.321\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eMales (bilateral asymmetry)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eFemales (bilateral asymmetry)\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle\u003c/p\u003e\n \u003cp\u003emass (kg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle thickness (mm)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle\u003c/p\u003e\n \u003cp\u003emass (kg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eMuscle thickness (mm)\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eAverage, 60\u0026deg;/s\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.406\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ePeak, 60\u0026deg;/s\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.245\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.317\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ens\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n \u003c/div\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec13\"\u003e\n \u003ch2\u003eMuscle mass estimation equation for the lower extremities\u003c/h2\u003e\n \u003cp\u003eStrong correlations were observed between the muscle mass and thickness parameters (Table \u003cspan\u003e3\u003c/span\u003e) in the jumping leg. Our aim was to find the strongest DEXA muscle mass prediction equation for the lower extremities based on anthropometric and ultrasonic measurements. By regarding the relationships between muscle mass (total and regional) and thickness in the anterior mid-thigh region (Table \u003cspan\u003e3\u003c/span\u003e, Fig. \u003cspan\u003e3\u003c/span\u003e), DEXA muscle mass could be estimated from muscle thickness and other muscular robustness predictors as well.\u003c/p\u003e\n \u003cdiv\u003e\n \u003ctable id=\"Tab3\" border=\"1\"\u003e\n \u003ccaption language=\"En\"\u003e\n \u003cdiv\u003eTable 3\u003c/div\u003e\n \u003cdiv\u003e\n \u003cp\u003ePearson correlation coefficients of the relations between the studied muscular robusticity and strength indicators (p\u0026thinsp;\u0026lt;\u0026thinsp;0.001 in both sexes and in all the studied relations)\u003c/p\u003e\n \u003c/div\u003e\n \u003c/caption\u003e\n \u003ccolgroup cols=\"8\"\u003e\u003c/colgroup\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003cth align=\"left\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\"\u003e\u0026nbsp;\u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eMuscle mass (total)\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eMuscle mass (jumping leg)\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eMuscle mass (opposite leg)\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eMuscle thickness -AM thigh (jumping leg)\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003eMuscle thickness -AM thigh (opposite leg)\u003c/p\u003e\n \u003c/th\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"5\"\u003e\n \u003cp\u003eBoys\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eMuscle mass (total)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" rowspan=\"4\"\u003e\n \u003cp\u003eGirls\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.963\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.972\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.664\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.596\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eMuscle mass (jumping leg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.961\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.968\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.666\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.603\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eMuscle mass (opposite leg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.962\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.959\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.642\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.586\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eMuscle thickness -AM thigh (jumping leg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.404\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.371\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.414\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.806\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003eMuscle thickness -AM thigh (jumping leg)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.345\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.287\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.318\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e0.778\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e-\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n \u003c/div\u003e\n \u003cp\u003eThe prediction of muscle mass in the jumping leg and in the whole body by using muscle thickness in the AM thigh, body mass and stature was significant in males, and revealed that more than 93% and 95%, resp. variability in muscle mass of the studied regions was accounted for these 3 predictors (Table \u003cspan\u003e4\u003c/span\u003e). In female athletes only body mass and muscle thickness in the AM thigh region were enough to predict muscle mass in the jumping leg or total body muscle mass: more than 91% and 94%, resp. of variability in muscle mass in the studied body regions was accounted AM thigh muscle thickness and body mass (Tables \u003cspan\u003e4\u003c/span\u003e\u0026ndash;5).\u003c/p\u003e\n \u003cp\u003e\u003cimg src=\"https://myfiles.space/user_files/122228_c8a1650c59388082/122228_custom_files/img1723809970.png\"\u003e\u003cbr\u003e\u003c/p\u003e\n \u003cdiv\u003e\n \u003cdiv align=\"left\"\u003e\u003cimg src=\"https://myfiles.space/user_files/122228_c8a1650c59388082/122228_custom_files/img1723809969.png\"\u003e\u003cbr\u003e\u003c/div\u003e\n \u003c/div\u003e\n\u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe muscle mass, thickness and strength in the studied body region of male handball players revealed an increase in puberty, and young adult male players muscular robusticity and strength increased after 10 years of age. Contrary to males, muscular robusticity and strength in females did not change intensively by age in jumping leg, female handball players seemed to reach their muscular strength and robusticity until the age of 14\u0026ndash;16. The strong association between muscle robusticity and strength in the thigh region was confirmed in males, and between muscle mass and strength in females, but not in muscle thickness in females in the studied group of young handball players.\u003c/p\u003e \u003cp\u003eAsymmetry is beneficial in special sports, however, increased bilateral asymmetry (asymmetry in skeleto-muscular robusticity, strength etc.), or the discrepancy from the sport-dependent, typical skeleto-muscular asymmetry may increase the injury risk and may decrease the physical performance in athletes. Experts suggest compensatory exercises for athletes if a higher ratio of robusticity or strength asymmetry is discovered. Former studies revealed that a 10\u0026ndash;15% muscle robusticity or strength asymmetry in athletes is considered as an indicator of significant muscular unbalance that is associated with a higher risk of injuries [e.g. 13]. This tendency could be confirmed and if the non-jumping leg showed a 5\u0026ndash;10% overdevelopment compared to the jumping leg in male handball players. However, a protective effect of 5\u0026ndash;10% muscular robusticity dominance in favour of the jumping leg appeared in both sexes in the studied group of handball players. A certain amount (5\u0026ndash;10%) asymmetry in the muscular development of the lower extremities, the 5\u0026ndash;10% overdevelopment of the jumping comparing to the non-jumping leg, seemed to decrease the risk of leg injuries in this type of sports, when the jumps are so important among the movements, when the jumps with hard landings, rapid changes of movement, frequent contacts and collisions between players characterise the game [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. By considering the age differences in the structural and/or functional inter-limb asymmetry in young athletes, the results have been controversial: former studies revealed no differences or increasing asymmetry by age in the during the pubertal period around the onset of peak height velocity [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan additionalcitationids=\"CR16\" citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. The present study confirmed that inter-limb asymmetry did not change by age in young handball players in the studied age interval.\u003c/p\u003e \u003cp\u003eThe higher level of asymmetry in the functional parameters compared to the structural ones in the thigh region of the lower extremity was found in both sexes in young athletes. This trend might be explained by that beside the development of the anatomical structures several factors influence the development of the functional capacities, as the learning of sports skills, the development of the nervous system etc. Injuries of the lower extremities were more frequent in female than in male athletes (19% in males, 29.6% in females) in the studied sample of young elite handball players. An 5\u0026ndash;10% asymmetry in the muscular robusticity of the legs in favour of the jumping leg revealed protection against leg injuries in handball players (injury prevalence in the lower extremities by the asymmetry categories \u0026lt;-10%: males \u0026ndash; 23.1%, -10 \u0026ndash; -5%: males \u0026ndash; 27.3%, -5\u0026ndash;5%: males \u0026ndash; 20.8%, females \u0026ndash; 38.5%, 5\u0026ndash;10%: males \u0026ndash; 7.1%, females \u0026ndash; 25%, \u0026gt;\u0026thinsp;10%: males \u0026ndash; 18.2%, females \u0026ndash; 27.3%, chi\u003csup\u003e2\u003c/sup\u003e test, p\u0026thinsp;\u0026lt;\u0026thinsp;0.05 in both sexes).\u003c/p\u003e \u003cp\u003eA new predictive equation of muscle mass in the jumping leg and the total body from the muscle thickness in the anterior mid-thigh region of jumping leg was introduce by analysing the relationship between DEXA muscle mass estimations and ultrasonic measures of quadriceps femoris in the thigh. The muscle mass estimation based on ultrasonography (BodyMetrix BX-2000) of muscle layers could be a reliable, accurate radiation-free, quick and easy alternative of DEXA estimation that can serve regularly information on muscle robusticity. We have already started the examinations of muscle robusticity in the upper extremities and in the trunk to construct muscle mass estimation equations also for these body regions in athletes that require only ultrasound measurements of muscle layers.\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eMuscular asymmetry, i.e. interlimb asymmetry in robusticity, strength, coordination and motor control between right and left extremities in athletes is considered a risk factor for an increased level of sports injuries. The analyses of asymmetry in the structural and functional indices of muscle development in handball players aged 14\u0026ndash;20 were performed to serve information for a future screening method of inter-limb asymmetry profile of young athletes. Our further aim is to construct such a screening method by studying the relationship between muscle thickness, strength, injury prevalence in the mirror of the asymmetry profile of young athletes in the other body regions, too.\u003c/p\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003eLimitations\u003c/h2\u003e \u003cp\u003eBilateral strength measured by isokinetic test and muscular robusticity in the same muscle group are sometimes not be verified by functional tests of the studied body region, since other muscle groups might compensate the developmental differences, asymmetries between the two sides of the given body region. Therefore, isokinetic tests should be identified by the kinetic tests (e.g. jumping on a force platform). Kinetic tests were also performed in the studied sample of athletes, however, the comparison of kinetic and isokinetic tests did not fit the topic of the present manuscript.\u003c/p\u003e \u003cp\u003eMuscle mass was measured by DEXA for the whole lower extremity, not only for the thigh segment of the extremity. Although the correlation between the muscle mass in thigh region and the whole lower extremity is very high, this methodological limitation should be considered.\u003c/p\u003e \u003cp\u003eThe weak or missing association of the parameters of the unity of structure and extension strength in the anterior region of the thighs suggests that other effects (ration of the 2 types of muscle fibres, thigh and muscle length, tendon insertion morphology etc.) should be considered in the future analyses in the bigger sample of elite athletes. Furthermore, the level of fatigue and overtraining should be also considered in such analyses. Our aim is to increase the sample size and complete the analysis by collecting information on the above-mentioned variables in a subsample of athletes, and to develop a new method for the estimation of the level of overtraining by using endocrine-immune and physical performance predictors.\u003c/p\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAZs: research design, data collection, analysis, writing the article, conceptualization, supervision. FZsR-S: data collection, writing the article, conceptualization, visualization. CsJ-K: data collection, writing the article. LP: research design, data collection, analysis, writing the article, conceptualization, supervision. PB: research design, data collection, analysis, writing the article. IJ: analysis, writing the article, conceptualization. TSz: research design, data collection, analysis, writing the article, conceptualization, supervision. All authors have read and agreed to the submitted version of the manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis research received no external funding.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eInstitutional Review Board Statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe study was reviewed and approved by the Committee of the Hungarian Handball Federation in 2023 (approval No: 1/2023, Budapest, January 2023) and by the Committee of the Doctoral School of Biology, Eotvos Lorand University, Budapest, Hungary in July 2022.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eInformed Consent Statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWritten informed consent was obtained from the legal guardians of children, and assent was obtained from the children as well.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData Availability Statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe data presented in this study are available on request from the corresponding author (AZs).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflicts of Interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no conflicts of interest.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eFriedmann-Bette, B., Bauer, T., Kinscherf, R., Vorwald, S., Klute, K., Bischoff, D., M\u0026uuml;ller, H., Weber, M.A., Metz, J., Kauczor, H.U., \u0026amp; B\u0026auml;rtsch, P. Effects of strength training with eccentric overload on muscle adaptation in male athletes. \u003cem\u003eEur. J. Appl. Physiol.\u003c/em\u003e \u003cstrong\u003e2010\u003c/strong\u003e, \u003cem\u003e108\u003c/em\u003e, 821\u0026ndash;836. https://doi.org/10.1007/s00421-009-1292-2 \u003c/li\u003e\n\u003cli\u003eLegerlotz, K., Marzilger, R., Bohm, S., \u0026amp; Arampatzis, A. Physiological adaptations following resistance training in youth athletes\u0026mdash;a narrative review. \u003cem\u003ePediatr. Exerc. Sci.\u003c/em\u003e \u003cstrong\u003e2016\u003c/strong\u003e, \u003cem\u003e28(4)\u003c/em\u003e, 501\u0026ndash;520. https://doi.org/10.1123/pes.2016-0023 \u003c/li\u003e\n\u003cli\u003eMersmann, F., Bohm, S., Schroll, A., Boeth, H., \u0026amp; Duda, G.N., Arampatzis, A. Muscle and tendon adaptation in adolescent athletes: a longitudinal study. \u003cem\u003eScand. J. Med. Sci. Sports\u003c/em\u003e. \u003cstrong\u003e2017\u003c/strong\u003e, \u003cem\u003e27(1)\u003c/em\u003e, 75\u0026ndash;82. https://doi.org/10.1111/sms.12631 \u003c/li\u003e\n\u003cli\u003eKadri, M.A., Noe, F., Maitre, J., Maffulli, N., \u0026amp; Paillard, T. Effects of limb dominance on postural balance in sportsmen practicing symmetric and asymmetric sports: A pilot study. \u003cem\u003eSymmetry\u003c/em\u003e. \u003cstrong\u003e2021\u003c/strong\u003e, \u003cem\u003e13(11)\u003c/em\u003e, 2199. https://doi.org/10.3390/sym13112199 \u003c/li\u003e\n\u003cli\u003eHietamo, J., Parkkari, J., Leppanen, M., Steffen, K., Kannus, P., Vasankari, T., Heinonen, A., Mattila, V.M., \u0026amp; Pasanen, K. Association between lower extremity muscular strength and acute knee injuries in young team‐sport athletes. \u003cem\u003eTransl. Sports Med.\u003c/em\u003e \u003cstrong\u003e2020\u003c/strong\u003e, \u003cem\u003e3(6)\u003c/em\u003e, 626\u0026ndash;637. https://doi.org/10.1002/tsm2.172 \u003c/li\u003e\n\u003cli\u003eMenzel, H.J., Chagas, M.H., Szmuchrowski, L.A., Araujo, S.R., de Andrade, A.G., \u0026amp; de Jesus-Moraleida, F.R. Analysis of lower limb asymmetries by isokinetic and vertical jump tests in soccer players. \u003cem\u003eJ. Strength Cond. Res.\u003c/em\u003e \u003cstrong\u003e2013\u003c/strong\u003e, \u003cem\u003e27(5)\u003c/em\u003e, 1370\u0026ndash;1377. https://doi.org/10.1519/JSC.0b013e318265a3c8 \u003c/li\u003e\n\u003cli\u003eTheodorou, E., Tryfonidis, M., \u0026amp; Zaras, N., Hadjicharalambous, M. Musculoskeletal Asymmetries in Young Soccer Players: 8 Weeks of an Applied Individual Corrective Exercise Intervention Program. \u003cem\u003eAppl. Sci.\u003c/em\u003e \u003cstrong\u003e2023\u003c/strong\u003e, \u003cem\u003e13(11)\u003c/em\u003e, 6445. https://doi.org/10.3390/app13116445 \u003c/li\u003e\n\u003cli\u003eLijewski, M., Burdukiewicz, A., Pietraszewska, J., Andrzejewska, J., \u0026amp; Stachon, A. Asymmetry of Muscle Mass Distribution and Grip Strength in Professional Handball Players. \u003cem\u003eInt. J. Environ. Res. Pub. Health.\u003c/em\u003e \u003cstrong\u003e2021\u003c/strong\u003e, \u003cem\u003e18(4)\u003c/em\u003e, 1913. https://doi.org/10.3390/ijerph18041913 \u003c/li\u003e\n\u003cli\u003eMadruga-Parera, M., Bishop, C., Beato, M., Fort-Vanmeerhaeghe, A., Gonzalo-Skok, O., \u0026amp; Romero-Rodriguez, D. Relationship between interlimb asymmetries and speed and change of direction speed in youth handball players. \u003cem\u003eJ. Strength Condit. Res.\u003c/em\u003e \u003cstrong\u003e2021\u003c/strong\u003e, \u003cem\u003e35(12)\u003c/em\u003e, 3482\u0026ndash;3490. https://doi.org/10.1519/JSC.0000000000003328 \u003c/li\u003e\n\u003cli\u003eBishop, C. Inter-limb Asymmetries: Are Thresholds a Usable Concept? \u003cem\u003eStrength Condit. J.\u003c/em\u003e \u003cstrong\u003e2021\u003c/strong\u003e, \u003cem\u003e43(1)\u003c/em\u003e, 32\u0026ndash;36. https://doi.org/10.1519/0000000000000554 \u003c/li\u003e\n\u003cli\u003eCadens, M., Planas-Anzano, A., Peirau-Ter\u0026eacute;s, X., Bishop, C., Romero-Rodr\u0026iacute;guez, D., \u0026amp; Madruga-Parera, M. Relationship between Asymmetry Profiles and Jump Performance in Youth Female Handball Players. \u003cem\u003eJ. Hum. Kin.\u003c/em\u003e \u003cstrong\u003e2023\u003c/strong\u003e, \u003cem\u003e88\u003c/em\u003e, 5\u0026ndash;16. https://doi.org/10.5114/jhk/163432 \u003c/li\u003e\n\u003cli\u003eKoo, T.K., Li, \u0026amp; M.Y. 2016. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. \u003cem\u003eJ. Chiropract. Med.\u003c/em\u003e \u003cstrong\u003e2016\u003c/strong\u003e, \u003cem\u003e15(2)\u003c/em\u003e, 155\u0026ndash;163. https://doi.org/10.1016/j.jcm.2016.02.012 \u003c/li\u003e\n\u003cli\u003eAsai, K., Nakase, J., Shimozaki, K., Toyooka, K., Kitaoka, K., \u0026amp; Tsuchiya, H. Incidence of injury in young handball players during national competition: A 6-year survey. \u003cem\u003eJ. Orthopaed. Sci.\u003c/em\u003e \u003cstrong\u003e2020\u003c/strong\u003e, \u003cem\u003e25(4)\u003c/em\u003e, 677\u0026ndash;681. https://doi.org/10.1016/j.jos.2019.06.011 \u003c/li\u003e\n\u003cli\u003eVargas, V.Z., Motta, C., Peres, B., Vancini, R.L., De Lira, C.A.B., \u0026amp; Andrade, M.S. Knee isokinetic muscle strength and balance ratio in female soccer players of different age groups: A cross-sectional study. \u003cem\u003ePhys. Sportsmed.\u003c/em\u003e \u003cstrong\u003e2019\u003c/strong\u003e, \u003cem\u003e48\u003c/em\u003e, 105\u0026ndash;109. https://doi.org/10.1080/00913847.2019.1642808 \u003c/li\u003e\n\u003cli\u003eRead, P., Oliver, J., Myer, G., De Ste Croix, M., \u0026amp; Lloyd, R. (2017). The Effects of Maturation on Measures of Asymmetry During Neuromuscular Control Tests in Elite Male Youth Soccer Players. \u003cem\u003ePediatr. Exerc. Sci.\u003c/em\u003e \u003cstrong\u003e2017\u003c/strong\u003e, \u003cem\u003e30(1)\u003c/em\u003e, 168\u0026ndash;175. https://doi.org/10.1123/pes.2017-0081 \u003c/li\u003e\n\u003cli\u003eMadruga-Parera, M., Romero-Rodriguez, D., Bishop, C., Beltran-Valls, M. R., Latinjak, A. T., Beato, M., \u0026amp; Fort-Vanmeerhaeghe, A. Effects of Maturation on Lower Limb Neuromuscular Asymmetries in Elite Youth Tennis Players. \u003cem\u003eSports\u003c/em\u003e. \u003cstrong\u003e2019\u003c/strong\u003e, \u003cem\u003e7(5)\u003c/em\u003e, 106. https://doi.org/10.3390/sports7050106 \u003c/li\u003e\n\u003cli\u003ePardos-Mainer, E., Bishop, C., Gonzalo-Skok, O., Nobari, H., P\u0026eacute;rez-Gomez, J., \u0026amp; Lozano, D. Associations between inter-limb asymmetries in jump and change of direction speed tests and physical performance in adolescent female soccer players. \u003cem\u003eInt. J. Environ. Res. Public Health. \u003c/em\u003e\u003cstrong\u003e2021\u003c/strong\u003e, \u003cem\u003e18(7)\u003c/em\u003e, 3474. https://doi.org/10.3390/ijerph18073474 \u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"
[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"young athletes, handball players, inter-limb asymmetry, strength and robusticity of the thigh","lastPublishedDoi":"10.21203/rs.3.rs-4743772/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4743772/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe relationship between structural and functional of parameters of skeletal muscles in young athletes needs further observations. The analyses of their age-group differences, sexual dimorphism, asymmetry characteristics in body regions, in sports having different pattern of physical loading could serve important information in this topic.\u003c/p\u003e \u003cp\u003e175 elite Hungarian handball players aged between 14 and 21 years were examined in 2023. Muscle mass component of the body segments was estimated by DEXA method and muscle thickness of the anterior mid-thigh region was measured by a new ultrasonic technique. The strength of knee extensor muscles was assessed by using an isokinetic protocol (Kineosystem dynamometer).\u003c/p\u003e \u003cp\u003eA strong association between muscle robusticity and strength in the thigh region was confirmed in males, but not in females. Asymmetry in muscle mass reflected in the asymmetry in the knee extensor strength. A new predictive equation of muscle mass in the jumping leg and the total body from the muscle thickness in the anterior mid-thigh region of jumping leg was introduced.\u003c/p\u003e \u003cp\u003eThe exploration and understanding of asymmetric structural and functional adaptations can help athletes and trainers in planning the training and training interventions to reduce the risk of injuries.\u003c/p\u003e","manuscriptTitle":"Muscular robusticity and strength in the lower extremities in elite handball players","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-08-16 12:14:12","doi":"10.21203/rs.3.rs-4743772/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"editorInvitedReview","content":"","date":"2024-08-18T14:59:47+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-08-09T12:33:35+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"196456461554095798735785183615884436451","date":"2024-08-05T08:07:17+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"16577897334928816216203771555168016465","date":"2024-08-05T05:11:07+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-08-05T04:54:35+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-08-04T12:12:55+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2024-07-23T17:36:06+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-07-22T11:50:47+00:00","index":"","fulltext":""},{"type":"submitted","content":"Scientific Reports","date":"2024-07-15T15:02:32+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"
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