Scapular Dynamic Muscular Stiffness Assessed through Myotonometry: A Narrative Review

Several tools have been used to assess muscular stiffness. Myotonometry stands out as an accessible, handheld, and easy to use tool. The purpose of this review was to summarize the psychometric properties and methodological considerations of myotonometry and its applicability in assessing scapular muscles. Myotonometry seems to be a reliable method to assess several muscles stiffness, as trapezius. This method has been demonstrated fair to moderate correlation with passive stiffness measured by shear wave elastography for several muscles, as well as with level of muscle contraction, pinch and muscle strength, Action Research Arm Test score and muscle or subcutaneous thickness. Myotonometry can detect scapular muscles stiffness differences between pre- and post-intervention in painful conditions and, sometimes, between symptomatic and asymptomatic subjects.


Introduction
Muscular stiffness, described as passive or dynamic [1][2][3], is a mechanical property that traduce the resistance offered to an action that leads to muscle tissue deformation [1,3]. More specifically, this muscular property derived from muscle structure and intrinsic material properties [4], namely from tendon [5], myofibrillar cross-bridges [5] (particularly titin filaments [6,7]) and muscular connective tissue [6]. The passive stiffness, commonly assessed with elastography methods [2,3], mainly represents the tissue adaptation [3] in it basal/passive status [8] and the baseline level of the stiffness [5]. The dynamic stiffness, assessed through myotonometry [9], is based on the free oscillation theory and results from the natural oscillation of the tissues, in response to a brief mechanical tap on the skin [10].
Both passive and dynamic stiffness are essential for adequate muscle contraction [7] and performance [11], as well as for adequate joint motor control [12] and integrity [13]. Muscle stiffness has been demonstrated to vary between subjects [14] according to age [12,15,16], muscle constitution, length, cross-sectional area [4,15] and measured point (myotendinous junction or muscle belly) [14]. Moreover, muscular stiffness has been demonstrated to be altered in conditions involving pain [17], injury [11], fatigue and cramps [18]. In pain conditions, the relevance of muscle stiffness in both movement and joint stability [19][20][21][22] • Programming the data acquisition: Introducing participant data (as weight, height, gender, and dominant side) [9] Sensors 2022, 22, 2565 3 of 19 II. Planning a "pattern composer", this is, defining an assessment protocol regarding the muscles to include and their condition of assessment (rest or contraction), the subject position and the measurements side, location and nº of repetitions [9] III.
Uploading the participant and assessment data to the myotonometry tool • The assessor should guarantee the equipment's stability and avoid the contact with external factors (as clothes) to not influence the device's impulses neither the tissues oscillations [9]; b. Coefficient of variation (total measurements' variability according to subject, assessor and device accuracy): should be lower than 3% [9]; c.
Measurement point: superficial reference of the muscles of interest, based not only in previous studies using myotonometry [48], but also researches using tools as algometer [25,48] and electromyography [4,48,49]. For repeated measurements, the same measuring points as well as same muscular and environmental conditions (as time of the day and subject's position), must be kept [9]; e.
Adjacent tissue: Measurement is only possible if the overlying subcutaneous fat is not higher than 20 mm [3,9,50]; f.

Validity
There is no gold standard of stiffness measurement in the literature, m comparisons to an accepted standard difficult [51,52]. In the absence of a criter measuring stiffness [51,52], the validity of the myotonometry tool has ofte determined by construct validity [51]. From these perspectives, myotonometry co

Validity
There is no gold standard of stiffness measurement in the literature, making comparisons to an accepted standard difficult [51,52]. In the absence of a criterion for measuring stiffness [51,52], the validity of the myotonometry tool has often been determined by construct validity [51]. From these perspectives, myotonometry construct validity was done by comparison it with several non-stiffness variables as: (a) level of muscle contraction, for rectus femoris of healthy subjects (r 2 = 0.9547) [52]; (b) static and dynamic strength measures, for soleus and lateral and medial gastrocnemius stiffness of healthy subjects [r = −0.81 to 0.48 (p < 0.05)] [53]; (c) lateral and palmar pinch strength and Action Research Arm Test score, for extensor digitorum and flexors carpi radialis and ulnaris of stroke patients [r = 0.25 to 0.52 (p < 0.05)] [54]; (d) muscle strength and muscle or subcutaneous thickness, for lower limb muscles of stroke patients [r = −0.84 to 0.46 (p < 0.05)] [55].
In turn, from the previously mentioned methods described to assess muscle stiffness, to our knowledge, only ultrasound shear wave elastography has been used to assess myotonometry validity.
The validation of myotonometry, particularly of Myoton as an instrument to measure muscular stiffness, by the correlation with this method when comparing muscular stiffness variables [1,4,18,49,56], has been done for several muscles [1,4,18,49,53,56], with different locations and functions [42,[57][58][59][60][61]. In this case, the correlation values ranged from −0.25 [1] to 0.71 [4] for healthy participants [1,4,18,49,56] (Table 1). Only one study reported no correlation between the two measures [1]. This study assessed relative changes in upper trapezius muscle stiffness between pre and post eccentric exercise. Despite the concurrent validity of myotonometry against elastography is the more frequently adopted approach, the differences between these two methods [1,3] should be considered in the analysis of the results presented in Table 1. Although both shear wave elastography and myotonometry use the principle of Young's modulus, the measured variable may depend on the method used [4]. The differences between the two methods are summarized in Table 2. There are variations such as the type of stiffness measured [dynamic or passive stiffness [1,3,62]], the depth of measurements [1] [superficial muscular stiffness measured with myotonometry, may not be comparable to the smaller and deeper measurements provided by shear wave [4]], but also in the related reliability of the variables measured [3,4,7,25,48,56,[63][64][65]. Table 2. Comparison between myotonometry and shear wave elastography for muscular stiffness assessment.

1.
Myotonometry presented lower coefficient of variability [4] and similar values of reliability compared to SWE 2.
Myotonometry present high to very high reliability for upper limb, lower limb and spine muscles [3,4,25,56] in healthy subjects, and low to very high reliability for UT in both healthy [7,21,25,48,63] or with a musculoskeletal disorder subjects [7]; while SWE present moderate to very high reliability for upper limb, lower limb and spine muscles [3,4,56,64,65] in healthy subjects.
The reliability values range from 0.229 [25], for UT, to 1 [4], for erector spinae. Specifically, regarding the scapular muscles and, in this case, the trapezius muscle, high to very high reliability were found for its three portions [7,21,25,48,63], with the exception of one study that reported a low to high reliability for the upper trapezius [25]. A more detailed description of reliability values for different muscles is presented in Table 3. As can be seen in Table 3, muscle stiffness assessment with myotonometry has been already studied in two muscular conditions, at rest and during contraction. The inclusion of these two conditions in muscle stiffness assessment protocols could be important given the dynamic characteristic of the soft tissues [74] and the influence of muscular length in the afferent inputs coming from muscle receptors [16]. Moreover, it could be useful to verify whether, particularly in subjects with conditions as pain, the relation of the muscle stiffness with the number of activated crossbridges is maintained [75].

Responsiveness
Responsiveness is a psychometric property traduce as the ability of an instrument to detect a meaningful change, in a clinical state, over time [54,76]. Regarding myotonometry, only one study was inferred about this property [54], demonstrating that the extensor digitorum, the flexor carpi radialis, and the flexor carpi ulnaris dynamic stiffness in stroke patients improved after intervention (robot-assisted training, mirror therapy, mirror therapy with mesh-glove electrical stimulation, or conventional rehabilitation). In the mentioned study [54], great sensitivity for change was found for the affected limb (−0.71 to −0.83) but not responsiveness for the unaffected limb (−0.42 to −0.48).
Previous studies regarding myotonometry, had already presented muscular assessment point references for the trapezius portions [7,12,21,25,[87][88][89] (Table 4 and Figure 3). However, a study about a 3D model construct through magnetic resonance [90] recommended other superficial references for upper trapezius, which might also be interest to consider given the possibility of considering some fibers with a more vertical orientation [79,90,91] compared with the "traditional" reference that possibly represent fibers with horizontal orientation [91,92] and higher cross-sectional area [91] (Table 4 and Figure 3). In addition, some studies [1,14,63] that assessed UT stiffness, measured this outcome through a grid of measurement points covering an extended area of UT muscle. Thus, considering the distance between C7 spinous process and the acromion several measurement points, separated by 1/6 [1,14,63] and/or 1/7 [14,63] of the mentioned distance, were defined. These measurement points include both muscle belly and myotendinous sites once muscle stiffness could be dependent on the location of the measurement point [1,63] (Figure 4).

Lower Trapezius
Mid-way from T6 spinous process to the medial border of spine of the scapulae [25] OR Mid-point of the lateral border of the fibers of lower trapezius [25] The superficial references for serratus anterior assessment with surface electromyography [93][94][95][96] could be considered for myotonometry assessment, once studies with ultrasound or magnetic resonance imaging [97][98][99] report thickness values similar to the trapezius muscle [97,98,[100][101][102], from 4.3 mm at rest to 11.8 mm while contracting [99]. Moreover, the studies about muscular thickness reported that lower trapezius is the thinner scapular muscle, ranging from 3.9 mm at rest [102] to 9.3 mm while contracting [98]. The fact that the myotonometry probe is placed on the assessment point, for each assessment repetition, with the patient already in the assessment position, also avoids the bias related to the proximity of the latissimus dorsi or pectoralis major [93] or to the geometric displacement (given skin movement during upper limb motions) [103] that could happen during surface electromyography [93]. As in the case of upper trapezius, serratus anterior could benefit form being assessed in two different portions, the upper/middle [93,94,96] given its role in the scapular protraction [93] and the lower [93], given its higher participation in scapular upward rotation [93,103] (Table 5 and Figure 5).

Levator scapulae
Between the posterior margin of sternocleidomastoid and anterior margin of the upper trapezius [104][105][106][107], at level of C4/5 [90] SA upper/middle portion Over the fourth rib, at the midpoint between the latissimus dorsi and the pectoralis major [93,94] SA lower portion Over the seventh rib, in the midline of the axilla [93], for SA lower portion (SAlow) [93] SA upper/middle portion Over the fourth rib, at the midpoin latissimus dorsi and the pectoralis

SA lower portion
Over the seventh rib, in the midlin for SA lower portion (SAlow) [93]  In its turn, the assessment of muscular stiffness of levator scap minor, that was already done with shear wave elastography [22,64,7 have been done with myotonometry given that these muscles are [19,110]. However, considering that a reference to the assessment of been used to collect surface electromyography [90,104,105] and that from 4.15 mm at rest to 6.38 mm while contracting [101,111], this musc requirements for myotonometry assessment (Table 5 and Figure 3 studies are required to confirm this possibility. In its turn, the assessment of muscular stiffness of levator scapulae and pectoralis minor, that was already done with shear wave elastography [22,64,72,108,109], may not have been done with myotonometry given that these muscles are deeper positioned [19,110]. However, considering that a reference to the assessment of levator scapulae has been used to collect surface electromyography [90,104,105] and that it thickness ranges from 4.15 mm at rest to 6.38 mm while contracting [101,111], this muscle seem to fulfill the requirements for myotonometry assessment (Table 5 and Figure 5). However, future studies are required to confirm this possibility.

Myotonometry Ability for Measuring Differences or Changes in Muscular Stiffness in Pain Conditions Involving Scapular Muscles
The relevance of scapular muscle stiffness to the shoulder complex and the possible muscle's stiffness changes resulting from the scapular position and their influence in muscular length [64] had led to the development of studies comparing trapezius stiffness, measured through myotometry, for between group comparisons as well pre and post intervention comparison [14,26,66,68,77,78].
UT stiffness was compared between subjects, or body sides, with and without pain conditions (Table 6). While two studies [26,77] reported significant differences between groups, by comparing subjects with different upper trapezius pain levels (0 to 3 in VAS) [26] or by comparing symptomatic and asymptomatic moderate neck pain subjects [77], 3 other studies found no differences in UT stiffness both between pain and healthy subjects [14,66,68] and between the affected and the non-affected extremity of the same subject [66,68].
The trapezius stiffness comparison of pre-and post-intervention moments has already been made for several rehabilitation techniques (Table 6). Four studies [14,25,68,78] report significant differences between the assessment moments traduced into a reduction of UT stiffness after treatment. However, the opposite results were found by Sokk et al. [66] for UT stiffness and by Kisilewicz et al. [25] considering MT and LT stiffness. Table 6. Myotonometry ability to identify differences or changes in scapular muscles stiffness in pain conditions ( for p < 0.05; X for p > 0.05) and the respective groups, muscle assessed and values of muscle stiffness (mean and SD) and p value.

Points That Need to Be Addressed in Future Studies
The summary of the information gathered in this review is presented in Figure 6. However, despite the several studies mentioned in the present review and their different aims, future studies regarding myotonometry, particularly for scapular muscles are still needed. Specifically, studies assessing the following issues are required: • Myotonometry assessment of serratus anterior and levator scapulae muscles are needed to validate the purposed assessment points, to define the myotonometry psychometric properties considering these muscles and to increase the knowledge about these muscles' mechanical properties.

•
The myotonometry psychometric properties should also be researched in subjects with different conditions, such as pain.

•
The use of myotonometry not only at rest condition but also during contraction, could bring new information that could help to standout adaptations in muscle stiffness modulation, given the muscular activity required and variation in the range of motion used in this muscular condition [112][113][114].

•
In studies with the intention to infer about intervention effects, the inclusion of follow-up moments could help to understand whether stiffness changes will be kept over time.

322
The present narrative review has limitations. First, for being a narrative review, the 323 present study could present some possible bias given the absence of predefined 324 hypothesis and protocol-based (also considering data extraction and synthesis), the lack 325 of necessity of following guidelines (as the ones purposed by PRISMA) or to the reduced 326 database consulted during search. Although this review presents the guidelines for the 327 correct use of myotonometry, it should be considered that these are specific for one 328 equipment. Moreover, given the equipment limitation regarding the possible interference 329 Figure 6. Summary of narrative review information regarding scapular dynamic muscular stiffness assessment through myotonometry and identification of the issues to be considered in future studies (LS: levator scapulae; LT: lower trapezius; MT: middle trapezius; SA: serratus anterior; UT: upper trapezius). The aspects that should be considered in future studies are summarized in Figure 6.

Study Limitations
The present narrative review has limitations. First, for being a narrative review, the present study could present some possible bias given the absence of predefined hypothesis and protocol-based (also considering data extraction and synthesis), the lack of necessity of following guidelines (as the ones purposed by PRISMA) or to the reduced database consulted during search. Although this review presents the guidelines for the correct use of myotonometry, it should be considered that these are specific for one equipment. Moreover, given the equipment limitation regarding the possible interference of subcutaneous fat, it would be important in future studies consider the measurement of subcutaneous fat in the specific measurement point of each muscle of interest as a criteria to use myotonometry.

Conclusions
The advantages of myotonometry together with the well-defined guidelines, the mostly high to very high values of reliability, the inferred responsiveness regarding the affected limb of stroke patients and its possible applicability to assess different scapular muscles stiffness, seems to support its use as a non-invasive method in the assessment of muscular mechanical properties as stiffness (N/m), for clinical practice or research. However, caution should be taken given the variable or no correlation with elastography, even if this may be justified by differences in the outcome measured.