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article 2024 12 pages

The Myometric Assessment of Achilles Tendon and Soleus Muscle Stiffness before and after a Standardized Exercise Test in Elite Female Volleyball and Handball Athletes—A Quasi-Experimental Study

Claudia Römer, Julia Czupajllo, Bernd Wolfarth, Freddy Sichting, Kirsten Legerlotz

Journal
Journal of Clinical Medicine
DOI
10.3390/jcm13113243
Publication type
Original Research
Study type
quasi-experimental study
Population
elite female volleyball and handball athletes
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Abstract

d:The high prevalence of injuries in female athletes necessitates a course of action that not only enhances research in this field but also incorporates improved prevention programs and regular health monitoring of highly stressed structures such as tendons and muscles. Since myometry is already used by coaches and physiotherapists, it is important to investigate whether tissue stiffness varies in different types of sports, and whether such measures are affected by an acute training session.Methods:Myometric measurements of the Achilles tendon (AT) and soleus muscle (SM) were performed in the longitudinal plane and relaxed tendon position. In total, 38 healthy professional female athletes were examined, applying a quasi-experimental study design, with subgroup analysis performed for different sports. To investigate the stiffness of the AT and SM, 24 female handball and volleyball athletes performed a standardized maximal incremental performance test on a treadmill. In this subgroup, myometric measurements were taken before and after the exercise test.Results:The measurements showed no significant difference between the mean pre- (AT: 661.46 N/m; SM

study design, with subgroup analysis performed for different sports. To investigate the stiffness of the AT and SM, 24 female handball and volleyball athletes performed a standardized maximal incremental performance test on a treadmill. In this subgroup, myometric measurements were taken before and after the exercise test.Results:The measurements showed no significant difference between the mean pre- (AT: 661.46 N/m; SM 441.48 N/m) and post-exercise stiffness (AT: 644.71 N/m; SM: 439.07 N/m). Subgroup analysis for different types of sports showed significantly lower AT and SM stiffness in swimming athletes compared to handball (p= 0.002), volleyball (p= 0.000) and hammer throw athletes (p= 0.008).Conclusions:Myometry can be performed on the same day as an acute training session in healthy female professional volleyball and handball athletes. Female swimmers have significantly lower AT and SM stiffness compared to female handball, volleyball and hammer throw athletes. These results show that the stiffness differences in the AT and SM can be assessed by myometry. Keywords:myometry; tendon; muscle; professional female athlete; type of sport 1. Introduction In 2024, there will be parity between women and men at the Olympic Games in Paris for the first time [1]. Despite this outstanding development in elite sport, women in competitive sports continue to face major challenges at the youth and adult ages due to a less well-developed health infrastructure. Disparities in funding and resources for professional female athletes not only lead to a gender data gap in research but also result in less access to high-quality sports medical care, diagnostics and strength and stability coaches. Furthermore, a lack of data on injury prevention programs among women in competitive sports still exists [2]. Specialists in sports medicine, as well as menstrual health management and mental health specialists, are necessary in a female athlete’s career to address early issues such as pre-menstrual syndrome or pregnancy-related concerns. Poorly developed prevention structures in professional female sports and lower remuneration often lead to J. Clin. Med.2024,13, 3243.

athlete’s career to address early issues such as pre-menstrual syndrome or pregnancy-related concerns. Poorly developed prevention structures in professional female sports and lower remuneration often lead to J. Clin. Med.2024,13, 3243.

J. Clin. Med.2024,13, 3243 2 of 12 rudimentary medical and physiotherapeutic care compared to male competitive athletes. Myometry is already used in competitive and recreational sports to measure differences in stiffness in various musculoskeletal tissues [3–5], and it may help close this data gap. 1.1. Myometry Application and Measurement The handheld device for myometry, MyotonPro (MyotonPro ® , Myoton AS, Tallin, Estonia), is easy to use and can be operated by non-medical personnel. It measures the oscillation response of musculoskeletal tissue via a standardized external impulse (force 0.4 N). The integrated accelerometer measures the oscillation and displays the oscillation curve and stiffness (N/m) on the screen [6]. The correct contact pressure is indicated to the examiner by means of color-coded light. The measurement can be performed quickly and in the same standardized examination position at the examination site or in physiotherapy. 1.2. Myometry in the General Population Myometry demonstrates good intra- and inter-rater reliability for muscles and ten- dons [7–12]. Data indicate a good between-day reliability for the lower limb in healthy elderly men [7] and a moderate to high reliability for passive and active contractions [12]. Specifically for the Achilles tendon (AT), there is high intra- and inter-rater reliability [5,13]. Furthermore, myometry shows significant differences in AT stiffness at different angles of dorsiflexion [14]. Like other stiffness assessment techniques, such as shear wave elas- tography, myometry can also detect stiffness differences in the AT and SM in different ankle positions [15,16], and it shows significantly higher stiffness in voluntarily contracted muscles compared to those at rest in healthy individuals [11]. Using myometry, age-related correlations were identified by Gervasi et al. [17]. Older sedentary controls exhibited higher values of dynamic stiffness (N/m) compared to active controls [17]. In an identical twin study, myometry detected significantly higher Achilles tendon stiffness in the recreationally active twin compared to the inactive one [18]. It was also shown that AT stiffness adaptation could be specific to the sport type [18] due to different locomotion patterns. 1.3. Myometry in Sports Myometry can be applied in sports to detect significant stiffness differences in the mus- culoskeletal

twin study, myometry detected significantly higher Achilles tendon stiffness in the recreationally active twin compared to the inactive one [18]. It was also shown that AT stiffness adaptation could be specific to the sport type [18] due to different locomotion patterns. 1.3. Myometry in Sports Myometry can be applied in sports to detect significant stiffness differences in the mus- culoskeletal tissue of symptomatic athletes, which can be indicative oftendinopathy [19,20] . Male athletes have been included more frequently in recent studies [4,21–24] and myometry data for professional female athletes in different type of sports are still lacking. Pruyn et al. conducted a study to assess muscle and tendon stiffness using myometry in female athletes at different competition levels [25]. Elite team sport players exhibited higher active stiffness compared to sub-elite players. These findings provide important insights into gender-specific stiffness and further research is necessary to evaluate myometry for more regular use in female sports. Pruyn et al. examined 15 female netball players and showed the good in-between-day reliability of myometry for athletes who avoided training sessions 24 h before measurement [26]. Data before and after acute exercise for professional female athletes, which could evaluate whether a single training session causes differences in dynamic stiffness measured by myometry, remain unavailable. The primary aim of this study is to examine the dynamic stiffness (N/m) of the Achilles tendon and soleus muscle in healthy female professional athletes before and after a standardized treadmill performance test using myometry. This study analyzes how a maximal training session influences muscle and tendon stiffness measured by MyotonPro. Thus, data for the AT and SM of professional female athletes with a comparable training load were measured before and compared to the data after a treadmill test. As Achilles tendinopathy shows a high prevalence in professional athletes [27], better preventive programs are crucial for reducing acute and chronic injuries. As MyotonPro is a handheld, easy-access tool for collecting quantitative data on musculoskeletal tissue,

tendinopathy shows a high prevalence in professional athletes [27], better preventive programs are crucial for reducing acute and chronic injuries. As MyotonPro is a handheld, easy-access tool for collecting quantitative data on musculoskeletal tissue,

J. Clin. Med.2024,13, 3243 3 of 12 data could be collected more regularly, thereby enhancing preventive programs for female professional athletes. The second aim of this study is to examine potential differences in stiffness between different types of sports and determine whether these can be measured by myometry. The study will assess the muscle and tendon stiffness of the soleus muscle and Achilles tendon. Given that different sports exhibit highly varied locomotion patterns, it is necessary to establish baseline values for professional female athletes. These baseline values may provide better insights into the development of tendinopathy by regular measurements of the muscle–tendon unit. By examining these parameters, this study aims to provide a deeper understanding of relevant biomechanical properties across different types of sports. This may enhance the comprehension of sport-specific performance and injury mechanisms by analyzing quantitative myometry data. The novelty of this study is its focus on myometry of the AT and SM in professional female athletes, as previous studies predominantly analyzed male athletes. The findings of this study may offer insights into gender- and sport-specific differences in tendon and muscle stiffness, which is essential for improving musculoskeletal prevention. 2. Methods 2.1. Study Design A quasi-experimental design was employed to investigate stiffness changes in the AT and SM before and after a standardized treadmill test, as measured by myometry. Due to the study design, no randomization was performed. Twenty-four female athletes (volleyball and handball) underwent a standardized exercise test on a treadmill as part of the annual basic physical examination. Furthermore, this study analyzed differences in the type of sport (volleyballn= 13, handballn= 11; hammer thrown= 9; swimmersn= 5) by using myometry. Musculoskeletal tissue was examined to gain insight into the relationship between myometry and the type of sports, as well as the athletic performance in female professional athletes. The inclusion criteria were (I) healthy female professional athletes (>10 h training per week), (II) without any acute (>6 months) musculoskeletal, rheumatic or vascular comorbidities and no previous injuries of the Achilles tendon or soleus muscle, (III) who provided written informed consent to participate in the study. The athletes’

sports, as well as the athletic performance in female professional athletes. The inclusion criteria were (I) healthy female professional athletes (>10 h training per week), (II) without any acute (>6 months) musculoskeletal, rheumatic or vascular comorbidities and no previous injuries of the Achilles tendon or soleus muscle, (III) who provided written informed consent to participate in the study. The athletes’ baseline characteristics were recorded on the examination day. On the day of the measurements and treadmill exercise test, no training was performed before the exercise test or the measurements. The running protocol was conducted on a treadmill (T170 h/p/cosmos) with a 1% incline. The treadmill velocity began at 6 km/h and was increased by 2 km/h every 3 minutes. The protocol lasted 18 to 21 min until individual exhaustion. The heart rate was continuously measured via mobile electrocardiogram, while the blood pressure and blood lactate were measured every three minutes. The lactate threshold and individual anaerobic threshold were determined after measurement. The maximal oxygen consumption (VO2peak) was calculated by the Ergonizer software (Version 5, Freiburg, Germany). The blood lactate was measured using a C-Line Biosen analyzer by EKF Diagnostic (Barleben, Germany). 2.2. Myometry Examination Protocol A standardized protocol was applied for all the myometry measurements of the female athletes. The pre- and post-exercise measurements were performed on the same day. For the assessment of the Achilles tendon, the mid-portion stiffness was measured, which was identified by using ultrasound in advance. The participants were examined in a prone position with both feet hanging in a relaxed position over the examination couch. The leg position was maintained for the measurement of the soleus muscle (SM) insertion, which was detected by ultrasound and subsequently marked. The measuring points were initially marked to ensure the exact measuring points were used before and after the standardized running test.

J. Clin. Med.2024,13, 3243 4 of 12 2.3. Statistical Analysis The mean of two measurements is recommended in the literature for robust results [7] and was performed in this study. For 2 measurement points in 38 female athletes, including post-measurements for 24 athletes, a total of 248 myometry measurements were performed. Statistical analysis for systematic deviation was conducted. The measurements were examined for a normal distribution using the Kolmogorov–Smirnov test. The student t-test was used for further analysis. The pairedt-test was used to investigate the pre- and post-exercise subgroup analysis. The unpairedt-test was performed to examine differences between different types of sports. A significance level ofp< 0.05 was determined and all the statistical analyses was performed using SPSS software (IBM Corp., released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY, USA: IBM Corp.). Microsoft Excel software (Microsoft Excel, released 2019, Redmond, WA, USA) was used for the boxplot visualization. Descriptive statistical analyses of all the athletes and subgroups were examined and analyses of the pre- and post-exercise measurements were conducted. Furthermore, sub- group analysis of 38 female athletes was performed for different types of sports. Pearson correlation was conducted using SPSS to examine the body composition of all the female athletes. It was used to calculate the relationship between the AT and SM stiffness and the lactate parameters and VO2peak. The significance of the correlation was determined by calculating thep-value. 3. Results 3.1. Athletes’ Characteristics The mean age of all 38 athletes was 20.61 years and the mean BMI was23.49±2.95 kg/m 2 . Table measured by myometry, with the minimum and maximum ranges. The mean values of stiffness (N/m) measured by myometry, with the minimum and maximum ranges, were 387 (297.5–535.5) for the SM and 650.71 (860.5–411.5) for the AT. Seven athletes reported ACL ruptures in the past, and one of these seven athletes reported ACL ruptures on both sides. One athlete reported patellar tendon rupture. None stated Achilles tendon rupture, pain, swelling or deficits in ankle movement during running or jumping in the past six months. Muscle pain or soreness of the lower limbs was not reported.

the AT. Seven athletes reported ACL ruptures in the past, and one of these seven athletes reported ACL ruptures on both sides. One athlete reported patellar tendon rupture. None stated Achilles tendon rupture, pain, swelling or deficits in ankle movement during running or jumping in the past six months. Muscle pain or soreness of the lower limbs was not reported. One athlete took L- Thyroxin as a treatment for hypothyroidism. One athlete took a progesterone contraceptive pill and one athlete a combined contraceptive pill. No other medications were reported. Table 1.Baseline characteristics and stiffness values (N/m) of the Achilles tendon and soleus muscle before and after a standardized treadmill test for exercise subgroup (n= 24) (handballn= 11 and volleyballn= 13). Variable Exercise Subgroup (n= 24) Volleyball/VB (n= 13) Handball/HB (n= 11) p-Value VB vs. HB Age [years] 22.08 ±3.11 21.38 ±3.10 22.91 ±3.05 0.239 Height [m] 1.79 ±0.08 1.84 ±0.07 1.73 ±0.06 0.000 BMI [kg/m 2 ] 22.51±1.95 21.76 ±1.28 23.41 ±2.27 0.051 Max. speed [km/h] 14.87 ±0.98 14.44 ±0.87 15.39 ±0.87 0.015 Max. lactate [mmol/L] 9.22 ±2.08 8.50 ±2.05 10.15 ±2.01 0.158 Pre exercise AT Left 680.65 ±82.54 703.71 ±72.77 638.60 ±90.86 0.085 Right 659.93 ±59.01 690.05 ±43.42 632.86 ±56.67 0.016 SM Left 402.55 ±45.73 458.25 ±68.91 421.35 ±58.44 0.675 Right 441.48 ±65.61 411.75 ±61.62 402.75 ±36.03 0.189

J. Clin. Med.2024,13, 3243 5 of 12 Table 1.Cont. Variable Exercise Subgroup (n= 24) Volleyball/VB (n= 13) Handball/HB (n= 11) p-Value VB vs. HB Post exercise AT Left 668.88 ±94.78 657.50 ±110.27 654.750 ±105.81 0.953 Right 640.28 ±69.69 666.67 ±58.93 618.35 ±75.87 0.119 SM Left 386.48 ±57.59 381.96 ±63.27 392.36 ±54.65 0.677 Right 443.05 ±72.78 442.08 ±55.32 435.15 ±95.57 0.841 Delta Pre vs. Post p-value Pre vs. Post AT Left 11.77 0.427 Right 19.65 0.120 SM Left 16.07 0.236 Right 1.57 0.916 There was no significant difference in mean dynamic stiffness before and after acute exercise for the Achilles tendon and soleus muscle on both sides in the exercise group (Table). All the athletes (volleyballn= 13, handballn= 11; hammer thrown= 9; swimmers n= 5) conducted 7–10 sport-specific training sessions, with additional strength and stability training sessions. For further examination, a descriptive analysis was conducted for the subgroup (n= 24) that performed a standardized treadmill test to examine the changes in AT and SM stiffness resulting from acute exercise using myometry. Besides the descriptive parame- ters, metabolic and speed parameters (maximal speed in km/h, speed at the individual anaerobic threshold—speed at IAT in km/h) were collected during the lactate threshold test. The relative VO2peak (ml/kg/bodyweight) was calculated by the software to allow a comparison of physical fitness in the exercise group. 3.2. Results of Subgroup Analysis before and after a Standardized Treadmill Test The exercise group included 13 professional volleyball athletes and 11 professional handball athletes. There was no significant difference in the stiffness of the AT (left) and SM (left and right) between the volleyball and handball athletes. The handball athletes exhibited a significantly softer AT on the right side before the exercise test compared to the volleyball players. The handball athletes were significantly shorter; however, the BMI was comparable. The handball and volleyball players had comparable lactate maximum values and comparable lactate values at the IAT. The calculated relative VO2peak was significantly higher in the handball players (p= 0.007; HB: 48.75 vs. VB: 45.49 mL/min/kg/bodyweight). Furthermore, the maximum running speed was significantly higher in the handball players (Table). A

handball athletes were significantly shorter; however, the BMI was comparable. The handball and volleyball players had comparable lactate maximum values and comparable lactate values at the IAT. The calculated relative VO2peak was significantly higher in the handball players (p= 0.007; HB: 48.75 vs. VB: 45.49 mL/min/kg/bodyweight). Furthermore, the maximum running speed was significantly higher in the handball players (Table). A significant negative correlation of−0.552 (p< 0.01) was found between the max- imum lactate value and the measured stiffness of the soleus muscle. There was also a negative correlation between the maximum lactate value and the stiffness of the Achilles tendon, but without sufficient significance. There was no significant correlation between the relative VO2peak and the stiffness of the AT and SM. As expected, the running speed at the IAT correlated significantly (Pearson correlation 0.702;p< 0.01) with the relative VO2peak. 3.3. Results of Subgroup Analysis for Type of Sport The hammer throwers (n= 9) were significantly heavier and shorter compared to the swimmers (n= 5). There were no significant differences in age, BMI and height. The handball players had a significantly higher BMI (p= 0.044) compared to the swimmers. Differences between the handball and volleyball athletes are displayed in Table.

Description

This research assesses myometric stiffness in elite female athletes during a standardized exercise test.