Test-retest reliability and responsiveness of a comprehensive protocol for the assessment of muscle tone of the ankle plantar flexors in healthy subjects

Abstract

BACKGROUND:

There is no information about the reliability of a comprehensive way to assess muscle tone that contains the different dimensions that define or could influence it in the ankle plantar flexors.

OBJECTIVE:

To evaluate the relative and absolute test-retest intra-day and inter-day reliability of a comprehensive protocol for the assessment of muscle tone responsiveness of the ankle plantar flexors.

METHODS:

Twenty healthy volunteers completed the study. It was performed a methodological study protocol (SPIRITT). Assessments included passive resistive torque-to-ankle dorsiflexion at slow (10 ${}^{\circ}$ /s) and fast (180 ${}^{\circ}$ /s) velocities, muscle extensibility measured as passive dorsiflexion range of motion, maximum isometric force and surface electromyography. Three measures were taken with a one-hour (intra-day reliability) and a one-week (inter-day reliability) rest interval between sessions. Inter-session reliability was examined through typical percentage error (CV ${}_{\text{TE}}$ ), percentage of change in the mean and intraclass correlation coefficients (ICC).

RESULTS:

Passive resistive-torque using isokinetic showed better reliability (CV ${}_{\text{TE}}$ from 7.1% to 18.3% and ICC: 0.64 to 0.94) than variables obtained with electromyography (CV ${}_{\text{TE}}$ : 36.5% to 72.5%; ICC: 0.56 to 0.69) and intra-day reliability showed better results than inter-day reliability. Extensibility test and maximal isometric force showed a very good intra-day and inter-day reliability (ICC from 0.82 to 0.97).

CONCLUSION:

The comprehensive protocol of muscle tone assessment showed very good reliability. The protocol established provides a reliable tool to assess and characterise muscle status and the effect of therapeutic interventions.

Keywords

Isokinetic electromyographic activity muscle tone strength muscle stiffness

1. Introduction

Muscle tone has been defined as “the state of activity or tension of a muscle beyond that related to its physical properties” [1]. Furthermore, clinically, muscle tone is accepted as the resistance felt to externally imposed movements during a state of voluntary relaxation [2], resulting from the interaction of the intrinsic viscoelastic muscle properties (also called “passive tone”, “mechanical”, “non-reflex” or “EMG-silent” component) and neurogenic factors that are activated by stimuli, represented mainly as the tonic stretch reflex, also called “active tone”, “reflex tone” or “neurogenic tone” [3, 4].

Muscle tone is usually quantified in subjects with spasticity and other muscle tone disorders using isokinetic dynamometry and surface Electromyography (sEMG) [5]. Furthermore, these techniques are also considered a valid method to measure muscle tone in non-injured subjects [6]. However, only specific mechanical muscle properties, such as stiffness, are usually assessed in non-injured subjects. Considering this, both the whole muscle tone concept and specific stiffness are important aspects to measure in healthy subjects when studying neuromuscular physiology, muscle performance, or action mechanisms of several therapeutic interventions. However, there are no validated protocols and few reliability studies that specifically measure muscle tone or any of its components in non-injured subjects [7].

The potential usefulness of sEMG has been suggested as a complementary method to detect and quantify the reflex muscular response to passive mobilisation [3, 5, 8]. Although there have been some techniques described to measure this neuromuscular activity, which is different between passive mobilisation and reflex stiffness [3, 8], there are no reliability studies to validate these protocols. Furthermore, the sEMG technique reveals limitations in reliability and sensitivity to electrode location and type of muscle contraction [9, 10]. Muscle extensibility has been highlighted as an important characteristic within mechanical muscle properties [11, 12]. However, the implication of muscle extensibility on muscle tone or performance needs to be clarified [12, 13, 14]. Muscle extensibility is usually measured as the passive range of motion during stretching [11, 15]. However, the endpoint of the stretching depends on the protocol used, possibly influencing the reliability of the measure. Objective protocols to quantify muscle extensibility are necessary to validate the responsiveness to the therapeutic approach and to determine the relations between passive muscle properties and muscle function. Muscular performance has also been related to muscle tone and mechanical muscle properties [12]. The reliability of dynamometer devices in the assessment of the strength has been evaluated in several studies [16, 17, 18] and the focus has largely been on the knee joint [19, 20]. At the ankle joint, Webber et al. analysed the relative and absolute intra-rater reliability of different types of contractions (isometric, isotonic and isokinetic) for ankle dorsiflexion and plantarflexion, finding minimal detectable change scores [18].

There is no information about the reliability of a comprehensive way to assess muscle tone that contains the different dimensions that define or could influence it (resistance to passive movement at different velocities, electromyographic activity, strength and extensibility) in the ankle plantarflexors. The idea of having a valid and a reliable protocol to quantify non-injured muscle tone could be useful in the field of sports and performance, and also for clinical purposes, to better understand muscle tone disorders and to study experimental treatments in healthy subjects. Therefore, the purpose of this study was to evaluate the relative and absolute test-retest intra-day and inter-day reliability of a proposed protocol that included passive resistive torque at 10 and 180 ${}^{\circ}$ /s, electromyographic activity, muscle extensibility and maximal voluntary isometric force by using an isokinetic dynamometer and an electromyography device.

2. Method

2.1 Subjects

Twenty healthy volunteers (12 males and 8 females) with a mean age of 26.6 $\pm$ 6.9 years were recruited in the study. All subjects were between 18–45 years old and had signed an informed consent form that was previously approved by the Toledo Hospital Clinical Research Ethics Committee. Sample size was calculated from a previous [21] work, which analysed passive resistive torque-to-ankle dorsiflexion of healthy subjects using a Kin-Com dynamometer. The minimal number of subjects required to attain a power of 0.9 and an alpha level of 0.05 was calculated to be 11. The final sample was established as 20 subjects to prevent possible dropout and to increase the power of the study. Participants were recruited among students of the local university and hospital staff using non-probabilistic convenience sampling. The exclusion criteria included any history of ipsilateral lower limb severe injury or intervention (e.g. fracture, surgical intervention, etc.), pain or musculoskeletal injury in the previous month, peripheral or central nervous system disease, and changes in physical activity that would have affected muscle tone during the study.

2.2 Procedures

A repeated measures design was carried out to determine the intra-day and inter-day reliability. A week before the testing sessions commenced, the participants were familiarised with the testing procedures by simulating the testing conditions that were carried out during the experimental sessions. In addition, in order to ascertain the participants’ dominant limb, during this familiarisation session, all of the participants were required to undertake three tests: 1) jumping on one leg, 2) kicking a ball, and 3) climbing onto a stool with one leg according to [22] protocol. The limb used to do at least 2/3 tests was considered the dominant and the tests were carried out with this lower limb.

After the familiarisation protocol, each participant undertook the testing procedure on three different occasions, with a one-hour (intra-day reliability) and a one-week (inter-day reliability) rest interval between testing sessions. The experimental conditions (room temperature at 25 ${}^{\circ}$ C) were designed to avoid inter-tester variability and to reduce the influence of individual circadian rhythms on test data. The clinician was blinded to the test results from previous testing sessions.

Figure 1.

A: Schematic representation of the experimental procedures for passive resistive torque and muscle extensibility measurement. Subjects are seated with the hip placed at a 90 ${}^{\circ}$ position and the knee extended. B and C: For the measurement of the passive resistive torque the isokinetic device performs a passive mobilization from platarflexion (125 ${}^{\circ}$ ) to dorsiflexion (80 ${}^{\circ}$ ) and the resistance and EMG is recorded. This procedure is repeated 5 times at 10/s velocity (B) and 10 times at 180 ${}^{\circ}$ /s velocity (C). D: For the passive range of motion measurement, the passive mobilization is performed from plantarflexion (125 ${}^{\circ}$ ) to the maximum dorsiflexion angle that is set as the position of the ankle at which the isokinetic device detects a resistance of 200 N. Angle and EMG are recorded. E: Recording of the maximal isometric voluntary force of plantarflexion and EMG activity during 3 seconds. The subject’s foot was fixed at 5 ${}^{\circ}$ of plantarflexion (95 ${}^{\circ}$ ) in a foot plate connected to the isokinetic dynamometer. Grey lines corresponds to torque measurements and black lines corresponds to angle measurements. Represented data are a typical example of a single subject (female of 34 years old, #s13).

Initially, all volunteers were seated with the hip placed at a 90 ${}^{\circ}$ position, the knee extended and the ankle in a neutral position strapped to a footplate that was connected to a Kin-Com dynamometer (Chattanooga Group Inc.). Bipolar silver chloride coated surface electrodes (Delsys Inc. Signal Conditioning Electrodes v2.3, USA) were placed over the Gastrocnemius Medialis (GM) muscle according to the SENIAM protocol (www.seniam.org). A 2 cm ${}^{2}$ stainless steel ground electrode was placed over the patella. The assessment consisted of a warm-up period of 10 passive mobilisations, a passive resistive torque test at both slow (10 ${}^{\circ}$ /s) and fast (180 ${}^{\circ}$ /s) velocities, a passive range of motion (PROM) test, and a maximum isometric voluntary force (MIVF) test (see below) for all subjects. After the completion of the first assessment (set 1), the electromyographic electrodes were removed and the subjects had a one-hour break before reassessment. The electromyographic electrodes were then reapplied, and the subjects were repositioned on the dynamometer to perform the second assessment (set 2). One week later the assessments were performed again following the same protocols (set 3).

2.3 Assessment

2.3.1 Measurement of passive resistive torque

Triceps Surae passive resistive torque was quantified by measuring the resistance to passive ankle dorsiflexion at slow (10 ${}^{\circ}$ /s) and fast (180 ${}^{\circ}$ /s) velocity. It has been evidenced that slow mobilisations express non-neural resistance to passive movement based principally on the mechanical elements of muscles, while fast mobilisations represent total muscle stiffness, including reflex-mediated resistance [23, 24]. Each subject’s foot was moved from 35 ${}^{\circ}$ of plantarflexion (125 ${}^{\circ}$ ) to 10 ${}^{\circ}$ of dorsiflexion (80 ${}^{\circ}$ ) [23] (Fig. 1A). Due to higher velocities having more variability, five repetitions were made for the 10 ${}^{\circ}$ /s (Fig. 1B), and 10 repetitions for 180 ${}^{\circ}$ /s velocities (Fig. 1C).

2.3.2 Measurement of gastrocnemius muscle extensibility

Muscle extensibility has been considered as the ability of a muscle to extend to a predetermined endpoint [11]. To ensure objective and independent quantification of the passive range of motion (PROM) for ankle dorsiflexion, the Kin-Com dynamometer was employed to perform mobilisation at a constant velocity at 10 ${}^{\circ}$ /s, from 35 ${}^{\circ}$ of plantarflexion to the maximum ankle dorsiflexion position. The maximum dorsiflexion angle was set as the position of the ankle at which the Triceps Surae muscles generated a resistance of 200 N against the passive movement (Fig. 1D). Goniometric measurement of maximal ankle PROM, with the knee in full extension, has been considered to represent extensibility of the Gastrocnemius muscles [15, 25]. Subjects were instructed to press a panic button to stop the mobilisation if they felt moderate pain, but no subjects stopped the controlled movement. All participants were mobilised with the same velocity and at the same strength.

2.3.3 Maximal voluntary isometric force (MVIF)

The subject’s foot was fixed at 5 ${}^{\circ}$ of plantarflexion (95 ${}^{\circ}$ ) in a foot plate connected to the dynamometer. Subjects performed two trials of ankle plantarflexion (Fig. 1E). Each trial consisted of a 3s isometric MVIF with a 20 s period of rest between trials.

2.4 Data recording and analysis

Isokinetic device outputs were connected to an analogical-digital converter (Micro 1401-3; Cambridge Electronic Devices, CED, Cambridge, UK) and digitally monitored and further analyzed using the Spike 2 software package (version 5.03, Cambridge Electronic Devices, CED, Cambridge, UK). Quantification of ankle dorsiflexion peak force (N), measured as a passive resistive force at both slow and fast velocities, was registered to measure maximal resistance of the Triceps Surae muscles. The resistance integral (N.s), measured during mobilisation, was analysed to represent the energy accumulated in the stretched muscle. A mean of five repetitions for each measure was made for the 10 ${}^{\circ}$ /s velocity and for the 10 repetitions made at 180 ${}^{\circ}$ /s movement velocity. The angle at which PROM was recorded during ankle dorsiflexion was obtained directly from the dynamometer, while the mean of the peak force obtained for plantarflexion MVIF was calculated.

Surface EMG was recorded at a gain of 1 KHz with an in-built filter bandwidth between 20–450 Hz. Electromyographic data were collected via the analogical-digital converter to be synchronized with the mechanical parameters obtained from the isokinetic device. Further EMG offline analysis was made with the Spike 2 software. GM EMG data were obtained during the maximal isometric plantarflexion activation. The GM EMG response was registered during the slow and fast passive dorsiflexion mobilisations. EMG data were rectified, averaged and integrated for each contraction. EMG activity recorded during maximal isometric plantarflexion is presented in units of mV.ms. GM EMG activity recorded during slow and fast passive ankle dorsiflexion was normalised as a percentage of the maximal isometric plantarflexion activation level.

2.5 Statistical analysis

SPSS v. 17.0 software (SPSS Inc., USA) was used to perform the statistical calculations. The distributions of datasets were checked using the Kolmogorov-Smirnov test, which demonstrated that all data had a normal distribution ( $p>$ 0.05). Descriptive statistics, including means and standard deviations, were calculated for the variables. Statistical significance was defined at $p<$ 0.05.

The test-retest reliability for each variable was calculated with pairs of trials (set 2–set 1 and set 3–set 1) [26]. In addition, the following establishments of reproducibility in human performance were explored [26, 27]: i) A paired sample $t$ -test was performed to identify the change in the mean, the 95% confidence intervals (CI) and the standard deviation of the difference between intra-day (set 1 vs. set 2) and inter-day (set 1 vs. set 3) pairs of trials for each variable and ii) the precision of measurement was determined. This was done using the typical percentage error (within-subjects variation in percentage) [26]. The typical percentage error (as a coefficient of variation [CV ${}_{\text{TE}}$ ] and its 95% CI were calculated using the log-transformed data via the following formula: 100 ( $e^{s}-1$ ), where s is the typical error (standard deviation of the difference between pairs of trials/ $\sqrt{2}$ ). Logarithmic transformation of the data was performed and used to reduce the possible heteroscedasticity (when the difference scores demonstrate a trend toward larger values for participants at one end of the plot) of the raw data [27]. To interpret the CV ${}_{\text{TE}}$ values, the current study used the arbitrary value suggested by Stokes [28] with an analytical goal of 15% of below. In addition, a third aspect was explored: iii) Assessment of the relative reliability was achieved using an intraclass correlation coefficient (ICC) that indicates the error in measurements as a proportion of the total variance in scores. As a general rule, we considered an ICC over 0.90 as high, between 0.80 and 0.90 as moderate and below 0.80 as low [26]. The standard error of measurement (SEM) also provides a measure of variability but was primarily used for calculating the minimal detectable Change (MDC). We define the MDC as the 95% CI of error associated with repeated measurements and was determined by the formula: MDC $=$ 2.09 $\times$ $\sqrt{2}$ $\times$ SEM; where 2.09 value is the $t$ statistic associated with a 95% CI and 19 degrees of freedom ( $t_{0.025,19}$ ) [26]. Only differences between two measurements that exceed the MDC represent a real (non-error) change in scores for a subject [29].

3. Results

Paired $t$ -test analyses reported no significant differences between set 1 and set 2 (intra-day) or between set 1 and set 3 (inter-day) in all variables analysed in the passive resistive torque test at slow and fast velocities (Table 2), the gastrocnemius muscle extensibility test or the MVIF test (Table 2). Mauchly’s test of sphericity was not significant ( $p>$ 0.05) for all variables.

Table 2 shows descriptive statistics (mean values $\pm$ standard deviation) for each variable in the passive resistive torque test at slow and fast velocities. The variables registered with the isokinetic showed better reliability (CV ${}_{\text{TE}}$ from 7.1% to 18.3%; ICC from 0.64 to 0.94) than did the variables registered with the electromyographic device (CV ${}_{\text{TE}}$ from 36.5% to 72.5%; ICC from 0.56 to 0.69). Intra-day reliability (CV ${}_{\text{TE}}$ : 7.1% to 44.1%; ICC: 0.67 to 0.94) showed better results than inter-day reliability (CV ${}_{\text{TE}}$ : 9.4% to 72.5%; ICC: 0.56 to 0.84). The MDC was 17.5 N and 14.2 N for peak force in passive resistive movement at 10 ${}^{\circ}$ /s and 180 ${}^{\circ}$ /s, 27.6 N $\cdot$ s and 2.2 N $\cdot$ s for integrated force in passive resistive movement at 10 ${}^{\circ}$ /s and 180 ${}^{\circ}$ /s, and 33.8 and 15.1 for the integrated GM EMG normalized from plantar flexion MVC at 10 ${}^{\circ}$ /s and 180 ${}^{\circ}$ /s, respectively.

Descriptive statistics for each variable in the extensibility test and in the MVIF test are shown in Table 2. The intra-day and inter-day ICC for PROM in the gastrocnemius muscle extensibility test were high (0.97 and 0.90, respectively). PROM showed the best CV ${}_{\text{TE}}$ results (0.9 for intra-day reliability and 1.5 for inter-day reliability). The CV ${}_{\text{TE}}$ for all variables in the MVIF test ranged from 10.9% to 33.2%, with an ICC score higher than 0.82. The CV ${}_{\text{TE}}$ values in the maximal voluntary isometric force test were better for the peak plantarflexion force variable than for the integrated gastrocnemius electromyography variable. The MDC was 4.8 ${}^{\circ}$ for the passive range of motion, 139.0 N for the peak plantarflexion force and 0.07 mV $\cdot$ ms for the integrated GM EMG.

Table 1
Descriptive values, inference statistic and absolute and relative reliability statistics among intra-day and inter-day sessions in passive resistive movement at slow (10 ${}^{\circ}$ /s) and fast (180 ${}^{\circ}$ /s) velocities (data are mean $\pm$ SD for 20 healthy subjects)

Variable	Descriptive statistic (mean $\pm$ SD)				Intra and inter-day reliability (mean and 95% CI)
	Set 1	Set 2	Set 3		Mean difference	$P$ value	ICC	CV ${}_{\text{TE}}$
Gastrocnemius muscle extensibility
Passive range of motion ( ${}^{\circ}$ )	158.4 $\pm$ 7.3	159.1 $\pm$ 7.1	158.7 $\pm$ 7.3	Intra-day (2-1)	0.7 $\pm$ 2.0 ( $-$ 0.3 to 1.6)	0.162	0.97 (0.91 to 0.99)	0.9 (0.7 to 1.3)
				Inter-day (3-1)	0.3 $\pm$ 3.3 ( $-$ 1.39 to 1.94)	0.729	0.90 (0.74 to 0.96)	1.5 (1.2 to 2.3)
Maximal voluntary isometric force
Peak plantarflexion force (N)	607.7 $\pm$ 213.8	596.9 $\pm$ 206.9	642.2 $\pm$ 248.8	Intra-day (2-1)	$-$ 10.8 $\pm$ 70.2 ( $-$ 43.6 to 22.1)	0.500	0.94 (0.86 to 0.98)	11.5 (8.6 to 17.2)
				Inter-day (3-1)	34.5 $\pm$ 93.5 ( $-$ 9.3 to 78.2)	0.115	0.92 (0.80 to 0.97)	10.9 (8.2 to 16.4)
Integrated GM EMG (mv*ms)	0.21 $\pm$ 0.11	0.19 $\pm$ 0.11	0.20 $\pm$ 0.13	Intra-day (2-1)	$-$ 0.02 $\pm$ 0.05 ( $-$ 0.04 to 0.01)	0.128	0.90 (0.77 to 0.96)	20.8 (15.5 to 31.8)
				Inter-day (3-1)	$-$ 0.01 $\pm$ 0.07 ( $-$ 0.04 to 0.03)	0.680	0.82 (0.59 to 0.93)	33.2 (24.4 to 52)

Table 2

Descriptive values, inference statistic and absolute and relative reliability statistics among intra-day and inter-day sessions in passive range of motion and maximal voluntary isometric force tests (data are mean $\pm$ SD for 20 healthy subjects)

4. Discussion

This study was conducted to establish intra-day and inter-day reliability scores for a comprehensive method to assess muscle tone of the ankle plantar flexors. We have addressed, in an objective way, the main dimensions of muscle tone (strength, passive resistive force to slow-and-fast velocities, muscle extensibility and EMG activity). Although the reliability of these isolated measures has been previously investigated to assess passive muscle properties [7, 30], there are no standardised protocols that include the whole assessment of muscle tone, which is used often in the clinical context. The results of this study demonstrated that the parameters registered with the isokinetic device in all of the variables were associated with good relative intra-day reliability (all ICCs $>$ 0.83), as well as moderate relative reliability for the variables assessed with the isokinetic device in the inter-day reliability (all ICCs $>$ 0.64). However, lower values were observed with the EMG device in the intra- and inter-day reliability (ICCs between 0.56 and 0.90). Furthermore, high absolute reliability (from 0.9 to 16.4) was observed for intra- and inter-day reliability in the variables registered with the isokinetic device. Particular attention, however, should be focused on the EMG measurements that yielded low levels of absolute intra-day and inter-day reliability (from 20.8 to 56.9), and thus, future applications should be made with caution. These data can be used for clinical and research goals, but values must be defined so as to provide guidance in deciding whether an observed change upon reassessment is within the boundaries of assessment error or if there has been a true observed change [26].

Several methods for the measurement of musculotendinous stiffness have been used, such as hopping and oscillation tests [30], myotonometers [31], custom built devices [32] or manual dynamometers [33]. The application of a constant velocity stretching performed by a commercialised isokinetic dynamometer has been also used in other studies in healthy subjects [34, 35, 36] and in subjects with muscle tone disorders [23, 24]. However, there is a lack of consensus for the use of a standardised protocol, not only to assess muscle stiffness, but also to evaluate muscle efferent innervation and other mechanical passive properties that may characterise muscle tone [4, 6]. Dorsiflexion stiffness reliability results for the present study have been similar [32, 33] or better [37, 38] than the findings in other similar studies. In addition, the inclusion of a high velocity stretching (180 ${}^{\circ}$ /s) measure contributed to the registration of the neurogenic component that influences muscle tone [8]. Measurement protocols in which the aim is to give more information about muscle tone over and above passive muscle mechanical properties should include at least two slow-and-fast velocities during muscle stretching. Global results from this study support the idea that slow velocity measures are more reliable than are high velocities. This could be due to the generation of the stretch reflex at high velocities [6, 8]. However, specific results suggest that the “peak torque” measure is better for slow velocities, and the “integrated force”, which represents the total energy needed to perform the stretching, is more reliable during fast velocities.

EMG activity was recorded to quantify neurogenic components of muscle tone, mainly due to the tonic stretch reflex that theoretically is present in high velocity stretching but not during low velocity stretching [6, 24]. However, our results showed similar percentages of EMG activation at slow (10 ${}^{\circ}$ /s) and fast (180 ${}^{\circ}$ /s) mobilisations, suggesting that the stretch reflex threshold could be independent of the velocity applied. Although the stretch reflex threshold has been detected at 70 ${}^{\circ}$ /s [8], Pisano et al. [6] only evoked the stretch reflex in 54% of healthy subjects when evaluating the stretching from 10 to 500 ${}^{\circ}$ /s. Regarding EMG reliability, integrated GM activity during maximal voluntary contraction had a very good intra- (0.90 ICC) and inter-session (0.82 ICC) reliability, similar to other studies with individuals who had normal muscles [39] and those with muscle tone disorders [40]. However, lower values were obtained when normalised during the passive stretching at both slow and fast velocities (0.56 to 0.69 ICC). Taking into account that these values were the lowest of the all measures from the whole protocol, other techniques or parameters, such as amplitude of the stretch reflex [8], reflex threshold [6] or percentage reflex gain [3] should be evaluated in future studies to improve this protocol.

Muscle extensibility is a critical dimension of muscle length and it is usually measured as maximal PROM [11, 15, 25]. However, there are several methods to quantify maximal dorsiflexion PROM [41] that mainly distinguish three types of endpoints where the mobilisation finishes: i) when the endpoint is determined by the examiner’s perception, usually as “firm resistance” [42]. This method does not usually measure the amount of applied torque required to perform the stretch, and the validity and reliability of this endpoint are highly questionable [11]; ii) when the endpoint is determined by the subject’s sensory perception. Although subject sensation is the most frequently used endpoint in human stretching research, there is little consensus regarding which sensation is most clinically relevant [11, 12]. The use of this method based on a sensory perception of stiffness has been criticised when evaluating passive muscle properties [11]; and iii) when the endpoint is defined by a specific amount of force or moment applied. The high reliability found in the present study and others [41, 43] suggests that applying the same amount of force to all subjects reduces the variability of subsequent readings between the same subjects and is a good method to quantify Triceps Suralis muscle extensibility. Although the relation between muscle extensibility and muscle stiffness has been suggested [13], no direct association has been evidenced [44].

Although several studies have calculated the reliability of isometric strength measurement using isokinetic dynamometers [18, 20], only some of them measured plantarflexion muscles, finding slightly lower ICCs [18, 45]. However, these studies evaluated older people and subjects with intermittent claudication. The measurement of the peak isometric plantarflexion force using an isokinetic dynamometer has a very good intra- (0.94, 0.86–0.98) and inter-day (0.92, 0.80–0.97) reliability.

There is a general controversy between the abstract concept of muscle tone, which is most used from a clinical perspective [46], and passive muscle properties, such as muscle stiffness, that are used in a biomechanics context. This could be confusing when both concepts are assessed with similar protocols based on passive resistive torque [6, 35]. However, muscle tone is also influenced by efferent innervation of the muscle (neurogenic component). This misunderstanding has also been observed using other measurement methodologies, such as myotonometers [31]. To avoid this, the proposed protocol in the present study suggests that muscle tone should be assessed in a comprehensive way, including other mechanical properties of the muscle, such as strength and extensibility, as well as the neurophysiological component using electromyography activity records.

Having a reliable and comprehensive protocol to quantify muscle tone and its associated components could be useful in several areas, such as to investigate the implications of muscle tone in sports performance, or to have healthy-experimental models to test new muscle tone disorders managements [34, 47]. Although more reliability studies are needed in specific populations, this comprehensive protocol is suitable to quantify muscle tone disorders such as contractures, hypertonia or spasticity. Furthermore, direct relations among muscle stiffness, extensibility and strength [13, 14, 44] and their role in muscle performance and task execution should be deeply studied. Moreover, other aspects such as the measures of responsiveness to change should also be addressed in future studies. The possibility of detecting the amount of change over time that is clinically relevant as a response to an intervention is an important key for validating these types of protocols [36].

One of the limitations of this study is that the measurement of the passive resistive torque was performed only at two velocities (slow and fast). It would be desirable to perform a wider range of velocities to have deeper information about both the neural mechanisms and the viscoelastic properties of muscle tone. However, the idea of the proposed protocol is to develop a practical and replicable procedure to measure muscle tone and adding more velocities would increase considerably the time required during each session. Another point to highlight is the pooled analysis of data in terms of gender or age. Expected differences in muscle tone could be found between genders or between young and old population and could bias the study. However, the idea of this study was to compare the measurements of each subjects with those performed by him/herself in a short period of time, and not to analyze the differences of gender or the influence of an intervention.

5. Conclusions

The comprehensive protocol of muscle tone measurement here tested, which includes passive resistive torque, muscle extensibility, strength and EMG activity, may represent a valid tool and has exhibited high reliability in quantifying muscle tone in non-injured subjects. Evaluation techniques that include multiple dimensions of muscle tone provide tools to better assess muscle status and the effect of therapeutic interventions. More studies are needed to understand muscle tone and its alterations, as well as more precise assessments, allowing for selection of the intervention that will best address the specific disorder or to assess the effects of training protocols in order to optimise the muscle status to performance.

Footnotes

Conflict of interest

The authors declare that they have no conflict of interest derived from the outcomes of this study. This study did not receive any funding.

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Test-retest reliability and responsiveness of a comprehensive protocol for the assessment of muscle tone of the ankle plantar flexors in healthy subjects

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Method

2.1 Subjects

2.2 Procedures

2.3.1 Measurement of passive resistive torque

2.3.2 Measurement of gastrocnemius muscle extensibility

2.3.3 Maximal voluntary isometric force (MVIF)

2.4 Data recording and analysis

2.5 Statistical analysis

3. Results

Table 1 Descriptive values, inference statistic and absolute and relative reliability statistics among intra-day and inter-day sessions in passive resistive movement at slow (10 ∘ /s) and fast (180 ∘ /s) velocities (data are mean ± SD for 20 healthy subjects)

5. Conclusions

Footnotes

Conflict of interest

References

Table 1
Descriptive values, inference statistic and absolute and relative reliability statistics among intra-day and inter-day sessions in passive resistive movement at slow (10 ${}^{\circ}$ /s) and fast (180 ${}^{\circ}$ /s) velocities (data are mean $\pm$ SD for 20 healthy subjects)