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Review

Scapular Dynamic Muscular Stiffness Assessed through Myotonometry: A Narrative Review

by
Ana S. C. Melo
1,2,3,4,
Eduardo B. Cruz
5,6,
João Paulo Vilas-Boas
3,7 and
Andreia S. P. Sousa
1,*
1
Center for Rehabilitation Research—Human Movement System (Re)habilitation Area, Department of Physiotherapy, School of Health, Polytechnic of Porto, Rua Dr. António Bernardino de Almeida, 400, 4200-072 Porto, Portugal
2
Research Centre in Physical Activity, Health and Leisure, Faculty of Sport, University of Porto, Rua Dr. Plácido Costa, 91, 4200-450 Porto, Portugal
3
Porto Biomechanics Laboratory (LABIOMEP-UP), University of Porto, Rua Dr. Plácido Costa, 91, 4200-450 Porto, Portugal
4
Center for Interdisciplinary Applied Research in Health, School of Health, Setubal Polytechnic Institute, Campus do IPS Estefanilha, 2914-503 Setubal, Portugal
5
Department of Physiotherapy, School of Health, Setubal Polytechnic Institute, Campus do IPS Estefanilha, 2914-503 Setubal, Portugal
6
Comprehensive Health Research Center (CHRC), Universidade Nova de Lisboa, 1169-056 Lisboa, Portugal
7
Centre of Research, Education, Innovation and Intervention in Sport (CIFI2D), Faculty of Sport, University of Porto, Rua Dr. Plácido Costa, 91, 4200-450 Porto, Portugal
*
Author to whom correspondence should be addressed.
Sensors 2022, 22(7), 2565; https://doi.org/10.3390/s22072565
Submission received: 7 March 2022 / Revised: 21 March 2022 / Accepted: 23 March 2022 / Published: 27 March 2022
(This article belongs to the Special Issue Sensors in Neurophysiology and Neurorehabilitation)
Browse Figures
Versions Notes

Abstract

:
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.

1. 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] highlight the possible influence of muscle stiffness deregulation, particularly in joints with high mobility like shoulder. Shoulder pain stands out for being a prevalent and recurrent of musculoskeletal condition [23,24] that involves stiffness adaptations in scapular muscles as upper trapezius (UT) [19,25,26]. These could be expected given the role of scapular muscles stiffness in shoulder stability [27] and function [28,29,30].
Muscle mechanical behavior has been studied for a long time [2,18]. In particular, muscular stiffness has been assessed by different non-invasive and reliable methods [1,2,3,4,18,31]:
(1)
elastography [magnetic resonance (MR) [2], ultrasound shear wave [2,3] or strain [3]];
(2)
tensiomyography [3];
(3)
myotonometry [3].
Among the different methods, the ultrasound elastography [shear wave or strain [3,18], which only perform a qualitative assessment based in a color scale [2,3,32]] and the MR elastography [2,31,33] have the advantage of combining the assessment of passive stiffness [1,2,3] with operator visualization of the structures of interest [18,33]. However, these methods are associated with high costs and requires specialized operator’s knowledge [3,18] and more assessment time [34]. In turn, tensiomyography assesses muscle stiffness by considering maximal radial displacement [3,35] in response to a stimulated contraction [3,36] and requires several tools as electrical stimulator, data acquisition subunit, probe, electrodes, tripod with manipulating hand, and laptop for software interface [35,37]. The disadvantages of the previously mentioned methods has led to an increased interest in less expensive [1,3,4], easier to use [1,3,4] and less dependent technical expertise tools [1,3,4] to assess muscle stiffness in different conditions of muscles contraction. Myotonometry has been developed to fulfil these needs [3] by assessing the dynamic stiffness [1,18] of superficial soft tissues [4,9,18,33].
Considering that different methods measure different stiffness related variables [3], the growing use of myotonometry as a consequence of its advantages and the need of easily and regularly assess muscle mechanical properties in the rehabilitation settings, a review of this assessment tool is needed. This is particularly relevant for scapular muscles, once their impairment [38,39,40,41,42] as already been related to the long-term recovery and recurrence of shoulder pain [41,42]. Moreover, the lack of effectiveness reported by some studies [29,43,44,45,46,47], regarding scapular therapeutic approaches for shoulder pain, particularly therapeutic exercises, could be related with the necessity of considering other outcomes in the patient assessment process. Thus, the present study aims to review the psychometric properties and methodological considerations of myotonometry to assess muscular stiffness, particularly of the scapular muscles. To fulfil this purpose, this review is organized in four sections. In the first section the methodological requirements and limitations of myotonometry is presented. This section is followed by a section presenting the myotonometry psychometric properties, including validity, reliability, and responsiveness. The third section review the myotonometry applicability for assessing scapular muscles stiffness by synthesizing the previous studies. Finally, the conclusion section highlights the advantages of myotonometry for the assessment of muscular stiffness but warns of the cautions that should be considered.

2. Guidelines to Myotonometry Measurements of Muscular Stiffness and Obtained Data

Several requirements and limitations should be considered when using myotonometry, particularly MyotonPRO digital palpation device (MyotonPro, Myoton AS, Tallinn, Estonia), to assess muscle stiffness (Figure 1):
  • Equipment:
    • Programming the data acquisition:
      • Introducing participant data (as weight, height, gender, and dominant side) [9]
      • 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]
      • 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];
  • Coefficient of variation (total measurements’ variability according to subject, assessor and device accuracy): should be lower than 3% [9];
  • Probe function: superficial tissues pre-compression followed by release of mechanical impulse and, consequently, muscular oscillation recording [1,3,4,9,18,43];
  • 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];
  • Adjacent tissue: Measurement is only possible if the overlying subcutaneous fat is not higher than 20 mm [3,9,50];
  • Eligible muscles: Superficial muscles [1,3,9], if bigger than 3 mm thickness and 20 g mass [9].
Myotonometry assesses muscle mechanical properties, particularly, muscle dynamic stiffness traduced as [3,9,18]:
Dynamic stiffness (N/m) = amax·mprobe/Δl
where amax represent the maximum amplitude of the acceleration of oscillation (mG); mprobe represent probe mass and Δl represent the maximum displacement of the tissue (mm) [9] (Figure 2).

3. Myotonometry Psychometric Properties Regarding the Measure of Muscular Stiffness

3.1. 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 (r2 = 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].

3.2. Reliability

Myotonometry reliability was already assessed for several muscles of different body segments [3,4,7,21,25,48,56,63]. Most studies only included healthy subjects [3,4,21,25,48,56,63], only one study included participants with musculoskeletal disorders in their sample [7].
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].

3.3. 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).

4. Applicability of Myotonometry for Assessing Scapular Muscles Stiffness

Several muscles have been assessed with myotonometry [1,4,7,14,18,25,49,56], however to our knowledge, among the scapular muscles, only the trapezius muscle has been assessed [1,7,14,21,25,26,63,66,68,77,78].
The trapezius is a standout muscle for scapular stabilization that act in a strong relation, mainly, with the major scapular mover—the serratus anterior [79]. In shoulder pain conditions, both have been reported as possibly altered, namely by decreased and/or timing changed activation of lower trapezius (LT), middle trapezius (MT) and serratus anterior (SA) [38,41,79,80] or by increased [38,39,40,41,42,79] or decreased UT activity [81,82,83]. Impairments in the activity of levator scapulae [19,84,85] and pectoralis minor [84,85,86] muscles were also reported.
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).
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).
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.

5. 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.
The aspects that should be considered in future studies are summarized in Figure 6.

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.

7. 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.

Author Contributions

Conceptualization, A.S.C.M., E.B.C., J.P.V.-B. and A.S.P.S., methodology, A.S.C.M., E.B.C., J.P.V.-B. and A.S.P.S., formal analysis, A.S.C.M.; investigation, A.S.C.M.; writing—original draft preparation, A.S.C.M. and A.S.P.S., writing—review and editing, A.S.C.M., E.B.C., J.P.V.-B. and A.S.P.S.; funding acquisition, A.S.C.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the under Grant SFRH/BD/140874/2018 and through R&D Units funding (UIDB/05210/2020), Fundação para a Ciência e Tecnologia (FCT), Portugal and the European Union (EU).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Kisilewicz, A.; Madeleine, P.; Ignasiak, Z.; Ciszek, B.; Kawczynski, A.; Larsen, R.G. Eccentric Exercise Reduces Upper Trapezius Muscle Stiffness Assessed by Shear Wave Elastography and Myotonometry. Front. Bioeng. Biotechnol. 2020, 8, 928. [Google Scholar] [CrossRef] [PubMed]
  2. Bilston, L.E.; Bolsterlee, B.; Nordez, A.; Sinha, S. Contemporary image-based methods for measuring passive mechanical properties of skeletal muscles in vivo. J. Appl. Physiol. 2019, 126, 1454–1464. [Google Scholar] [CrossRef] [PubMed]
  3. Bravo-Sánchez, A.; Abián, P.; Sánchez-Infante, J.; Esteban-Gacía, P.; Jiménez, F.; Abián-Vicén, J. Objective Assessment of Regional Stiffness in Vastus Lateralis with Different Measurement Methods: A Reliability Study. Sensors 2021, 21, 3213. [Google Scholar] [CrossRef] [PubMed]
  4. Kelly, J.P.; Koppenhaver, S.L.; Michener, L.A.; Proulx, L.; Bisagni, F.; Cleland, J.A. Characterization of tissue stiffness of the infraspinatus, erector spinae, and gastrocnemius muscle using ultrasound shear wave elastography and superficial mechanical deformation. J. Electromyogr. Kinesiol. 2018, 38, 73–80. [Google Scholar] [CrossRef]
  5. Blackburn, J.T.; Padua, D.A.; Riemann, B.L.; Guskiewicz, K.M. The relationships between active extensibility, and passive and active stiffness of the knee flexors. J. Electromyogr. Kinesiol. 2004, 14, 683–691. [Google Scholar] [CrossRef]
  6. Schleip, R.; Naylor, I.L.; Ursu, D.; Melzer, W.; Zorn, A.; Wilke, H.-J.; Lehmann-Horn, F.; Klingler, W. Passive muscle stiffness may be influenced by active contractility of intramuscular connective tissue. Med. Hypotheses. 2006, 66, 66–71. [Google Scholar] [CrossRef]
  7. Viir, R.; Laiho, K.; Kramarenko, J.; Mikkelsson, M. Repeatability of trapezius muscle tone assessment by a myometric method. J. Mech. Med. Biol. 2006, 6, 215–228. [Google Scholar] [CrossRef]
  8. Maïsetti, O.; Hug, F.; Bouillard, K.; Nordez, A. Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging. J. Biomech. 2012, 45, 978–984. [Google Scholar] [CrossRef]
  9. Myoton, A.S. MyotonPRO Digital Palpation—USER MANUAL, Desktop Software v 5.0.0.211. MYOTON AS; Tallinn, Estonia, 2020; pp. 1–115. Available online: www.myoton.com (accessed on 1 March 2022).
  10. Bravo-Sánchez, A.; Abián, P.; Jimenez, F.; Abián-Vicén, J. Structural and mechanical properties of the Achilles tendon in senior badminton players: Operated vs. non-injured tendons. Clin. Biomech. 2021, 85, 105366. [Google Scholar] [CrossRef]
  11. Bernabei, M.; Lee, S.S.M.; Perreault, E.J.; Sandercock, T.G. Shear wave velocity is sensitive to changes in muscle stiffness that occur independently from changes in force. J. Appl. Physiol. 2020, 128, 8–16. [Google Scholar] [CrossRef]
  12. Kocur, P.; Tomczak, M.; Wiernicka, M.; Goliwas, M.; Lewandowski, J.; Łochyński, D. Relationship between age, BMI, head posture and superficial neck muscle stiffness and elasticity in adult women. Sci. Rep. 2019, 9, 8515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Huxel, K.C.; Swanik, C.B.; Swanik, K.A.; Bartolozzi, A.R.; Hillstrom, H.J.; Sitler, M.R.; Moffit, D.M. Stiffness Regulation and Muscle-Recruitment Strategies of the Shoulder in Response to External Rotation Perturbations. J. Bone Jt. Surg. 2008, 90, 154–162. [Google Scholar] [CrossRef] [PubMed]
  14. Heredia-Rizo, A.M.; Petersen, K.K.; Arendt-Nielsen, L.; Madeleine, P. Eccentric Training Changes the Pressure Pain and Stiffness Maps of the Upper Trapezius in Females with Chronic Neck-Shoulder Pain: A Preliminary Study. Pain Med. 2020, 21, 1936–1946. [Google Scholar] [CrossRef] [PubMed]
  15. Eby, S.; Song, P.; Chen, S.; Chen, Q.; Greenleaf, J.F.; An, K.-N. Validation of shear wave elastography in skeletal muscle. J. Biomech. 2013, 46, 2381–2387. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Marusiak, J.; Jarocka, E.; Jaskólska, A.; Jaskólski, A. Influence of number of records on reliability of myotonometric measurements of muscle stiffness at rest and contraction. Acta Bioeng. Biomech. 2018, 20, 123–131. [Google Scholar] [PubMed]
  17. Hodges, P.W.; Tucker, K. Moving differently in pain: A new theory to explain the adaptation to pain. Pain 2011, 152 (Suppl. 3), S90–S98. [Google Scholar] [CrossRef] [PubMed]
  18. Feng, Y.N.; Li, Y.P.; Liu, C.L.; Zhang, Z.J. Assessing the elastic properties of skeletal muscle and tendon using shearwave ultrasound elastography and MyotonPRO. Sci. Rep. 2018, 8, 17064. [Google Scholar] [CrossRef]
  19. Ishikawa, H.; Muraki, T.; Morise, S.; Sekiguchi, Y.; Yamamoto, N.; Itoi, E.; Izumi, S.-I. Changes in stiffness of the dorsal scapular muscles before and after computer work: A comparison between individuals with and without neck and shoulder complaints. Eur. J. Appl. Physiol. 2017, 117, 179–187. [Google Scholar] [CrossRef]
  20. Leong, H.T.; Hug, F.; Fu, S.N. Increased Upper Trapezius Muscle Stiffness in Overhead Athletes with Rotator Cuff Tendinopathy. PLoS ONE 2016, 11, e0155187. [Google Scholar]
  21. Liu, C.; Feng, Y.; Zhang, H.; Li, Y.; Zhu, Y.; Zhang, Z. Assessing the viscoelastic properties of upper trapezius muscle: Intra- and inter-tester reliability and the effect of shoulder elevation. J. Electromyogr. Kinesiol. 2018, 43, 226–229. [Google Scholar] [CrossRef]
  22. Taş, S.; Korkusuz, F.; Erden, Z. Neck Muscle Stiffness in Participants With and Without Chronic Neck Pain: A Shear-Wave Elastography Study. J. Manip. Physiol. Ther. 2018, 41, 580–588. [Google Scholar] [CrossRef]
  23. Larkin-Kaiser, K.A.; Parr, J.J.; Borsa, P.A.; George, S.Z. Range of motion as a predictor of clinical shoulder pain during recovery from delayed-onset muscle soreness. J. Athl. Train. 2015, 50, 289–294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Luime, J.J.; Koes, B.W.; Hendriksen, I.J.; Burdorf, A.; Verhagen, A.P.; Miedema, H.S.; Verhaar, J.A. Prevalence and incidence of shoulder pain in the general population; a systematic review. Scand. J. Rheumatol. 2004, 33, 73–81. [Google Scholar] [CrossRef] [PubMed]
  25. Kisilewicz, A.; Janusiak, M.; Szafraniec, R.; Smoter, M.; Ciszek, B.; Madeleine, P.; Fernández-de-Las-Peñas, C.; Kawczyński , A. Changes in Muscle Stiffness of the Trapezius Muscle After Application of Ischemic Compression into Myofascial Trigger Points in Professional Basketball Players. J. Hum. Kinet. 2018, 64, 35–45. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Kim, J.; Hyong, I. Study on Change of Muscle Tone and Stiffness According to upper trapezius Mild Pain tf young Adults. Indian J. Public Health Res. Dev. 2018, 9, 605. [Google Scholar] [CrossRef]
  27. Yang, J.L.; Jan, M.H.; Hung, C.J.; Yang, P.L.; Lin, J.J. Reduced scapular muscle control and impaired shoulder joint position sense in subjects with chronic shoulder stiffness. J. Electromyogr. Kinesiol. 2010, 20, 206–211. [Google Scholar] [CrossRef] [PubMed]
  28. Moeller, C.R.; Bliven, K.C.; Valier, A.R. Scapular muscle-activation ratios in patients with shoulder injuries during functional shoulder exercises. J. Athl. Train. 2014, 49, 345–355. [Google Scholar] [CrossRef] [Green Version]
  29. Nodehi Moghadam, A.; Rahnama, L.; Noorizadeh Dehkordi, S.; Abdollahi, S. Exercise therapy may affect scapular position and motion in individuals with scapular dyskinesis: A systematic review of clinical trials. J. Shoulder Elbow Surg. 2020, 29, e29–e36. [Google Scholar] [CrossRef] [Green Version]
  30. Kara, D.; Harput, G.; Duzgun, I. Trapezius muscle activation levels and ratios during scapular retraction exercises: A comparative study between patients with subacromial impingement syndrome and healthy controls. Clin. Biomech. 2019, 67, 119–126. [Google Scholar] [CrossRef]
  31. Hong, S.H.; Hong, S.; Yoon, J.; Oh, C.; Cha, J.G.; Kim, H.K.; Bolster, B., Jr. Magnetic resonance elastography (MRE) for measurement of muscle stiffness of the shoulder: Feasibility with a 3 T MRI system. Acta Radiol. 2016, 57, 1099–1106. [Google Scholar] [CrossRef]
  32. Brandenburg, J.E.; Eby, S.F.; Song, P.; Zhao, H.; Brault, J.S.; Chen, S.; An, K.-N. Ultrasound Elastography: The New Frontier in Direct Measurement of Muscle Stiffness. Arch. Phys. Med. Rehab. 2014, 95, 2207–2219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Ringleb, S.I.; Bensamoun, S.F.; Chen, Q.; Manduca, A.; An, K.-N.; Ehman, R.L. Applications of magnetic resonance elastography to healthy and pathologic skeletal muscle. J. Magn. Reson. Imaging 2007, 25, 301–309. [Google Scholar] [CrossRef] [PubMed]
  34. Taş, S.; Yaşar, Ü.; Kaynak, B.A. Interrater and Intrarater Reliability of a Handheld Myotonometer in Measuring Mechanical Properties of the Neck and Orofacial Muscles. J. Manip. Physiol. Ther. 2020, 44, 42–48. [Google Scholar] [CrossRef] [PubMed]
  35. Sánchez-Infante, J.; Bravo-Sánchez, A.; Jiménez, F.; Abián-Vicén, J. Effects of dry needling on mechanical and contractile properties of the upper trapezius with latent myofascial trigger points: A randomized controlled trial. Musculoskelet. Sci. Pract. 2021, 56, 102456. [Google Scholar] [CrossRef]
  36. Lohr, C.; Schmidt, T.; Medina-Porqueres, I.; Braumann, K.-M.; Reer, R.; Porthun, J. Diagnostic accuracy, validity, and reliability of Tensiomyography to assess muscle function and exercise-induced fatigue in healthy participants. A systematic review with meta-analysis. J. Electromyogr. Kinesiol. 2019, 47, 65–87. [Google Scholar] [CrossRef]
  37. Park, S. Theory and usage of tensiomyography and the analysis method for the patient with low back pain. J. Exerc. Rehabil. 2020, 16, 325–331. [Google Scholar] [CrossRef]
  38. Cole, A.K.; McGrath, M.L.; Harrington, S.; Padua, D.; Rucinski, T.J.; Prentice, W.E. Scapular Bracing and Alteration of Posture and Muscle Activity in Overhead Athletes With Poor Posture. J. Athl. Train. 2013, 48, 12–24. [Google Scholar] [CrossRef] [Green Version]
  39. Moezy, A.; Sepehrifar, S.; Dodaran, M.S. The effects of scapular stabilization based exercise therapy on pain, posture, flexibility and shoulder mobility in patients with shoulder impingement syndrome: A controlled randomized clinical trial. Med. J. Islam. Repub. Iran 2014, 28, 87. [Google Scholar]
  40. Tsuruike, M.; Ellenbecker, T.S. Serratus anterior and lower trapezius muscle activities during multi-joint isotonic scapular exercises and isometric contractions. J. Athl. Train. 2015, 50, 199–210. [Google Scholar] [CrossRef] [Green Version]
  41. Magarey, M.E.; Jones, M.A. Dynamic evaluation and early management of altered motor control around the shoulder complex. Man. Ther. 2003, 8, 195–206. [Google Scholar] [CrossRef]
  42. Phadke, V.; Camargo, P.; Ludewig, P. Scapular and rotator cuff muscle activity during arm elevation: A review of normal function and alterations with shoulder impingement. Braz. J. Phys. Ther. 2009, 13, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Abdulla, S.Y.; Southerst, D.; Côté, P.; Shearer, H.M.; Sutton, D.; Randhawa, K.; Varatharajan, S.; Wong, J.J.; Yu, H.; Marchand, A.-A.; et al. Is exercise effective for the management of subacromial impingement syndrome and other soft tissue injuries of the shoulder? A systematic review by the Ontario Protocol for Traffic Injury Management (OPTIMa) Collaboration. Man. Ther. 2015, 20, 646–656. [Google Scholar] [CrossRef] [PubMed]
  44. Bury, J.; West, M.; Chamorro-Moriana, G.; Littlewood, C. Effectiveness of scapula-focused approaches in patients with rotator cuff related shoulder pain: A systematic review and meta-analysis. Man Ther. 2016, 25, 35–42. [Google Scholar] [CrossRef] [PubMed]
  45. Shire, A.R.; Stæhr, T.A.B.; Overby, J.B.; Dahl, M.B.; Jacobsen, J.S.; Christiansen, D.H. Specific or general exercise strategy for subacromial impingement syndrome-does it matter? A systematic literature review and meta analysis. BMC Musculoskelet. Disord. 2017, 18, 158. [Google Scholar] [CrossRef] [PubMed]
  46. Reijneveld, E.A.; Noten, S.; Michener, L.A.; Cools, A.; Struyf, F. Clinical outcomes of a scapular-focused treatment in patients with subacromial pain syndrome: A systematic review. Br. J. Sports Med. 2017, 51, 436–441. [Google Scholar] [CrossRef] [PubMed]
  47. van den Dolder, P.A.; Ferreira, P.H.; Refshauge, K.M. Effectiveness of soft tissue massage and exercise for the treatment of non-specific shoulder pain: A systematic review with meta-analysis. Br. J. Sports Med. 2014, 48, 1216–1226. [Google Scholar]
  48. Klich, S.; Pietraszewski, B.; Zago, M.; Galli, M.; Lovecchio, N.; Kawczyński, A. Ultrasonographic and Myotonometric Evaluation of the Shoulder Girdle After an Isokinetic Muscle Fatigue Protocol. J. Sport Rehabil. 2020, 29, 1047–1052. [Google Scholar] [CrossRef]
  49. Gözübüyük, Ö.B.; Tahirbegolli, B.; Isik, A. The correlation between myotonometer and elastography at measuring viscoelastic properties of muscle tissue. In Proceedings of the 10th European Sports Medicine Congress of EFSMA, Cascais, Portugal, 16–18 November 2017. [Google Scholar]
  50. Nair, K.; Masi, A.T.; Andonian, B.; Barry, A.J.; Coates, B.; Dougherty, J.; Schaefer, E.; Henderson, J.; Kelly, J. Stiffness of resting lumbar myofascia in healthy young subjects quantified using a handheld myotonometer and concurrently with surface electromyography monitoring. J. Bodyw. Mov. Ther. 2016, 20, 388–396. [Google Scholar] [CrossRef]
  51. Murphy, A.J.; Watsford, M.L.; Coutts, A.J.; Pine, M.J. Reliability of a test of musculotendinous stiffness for the triceps-surae. Phys. Ther. Sport 2003, 4, 175–181. [Google Scholar] [CrossRef]
  52. Zinder, S.M.; Padua, D.A. Reliability, validity, and precision of a handheld myometer for assessing in vivo muscle stiffness. J. Sport Rehabilitation 2011, 20, 1–8. [Google Scholar] [CrossRef] [Green Version]
  53. Pruyn, E.C.; Watsford, M.L.; Murphy, A.J. Validity and reliability of three methods of stiffness assessment. J. Sport Health Sci. 2016, 5, 476–483. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Chuang, L.-L.; Wu, C.-Y.; Lin, K.-C. Reliability, Validity, and Responsiveness of Myotonometric Measurement of Muscle Tone, Elasticity, and Stiffness in Patients with Stroke. Arch. Phys. Med. Rehabil. 2012, 93, 532–540. [Google Scholar] [CrossRef] [PubMed]
  55. Fröhlich-Zwahlen, A.; Casartelli, N.; Item-Glatthorn, J.; Maffiuletti, N. Validity of resting myotonometric assessment of lower extremity muscles in chronic stroke patients with limited hypertonia: A preliminary study. J. Electromyogr. Kinesiol. 2014, 24, 762–769. [Google Scholar] [CrossRef] [PubMed]
  56. Lee, Y.; Kim, M.; Lee, H. The Measurement of Stiffness for Major Muscles with Shear Wave Elastography and Myoton: A Quantitative Analysis Study. Diagnostics 2021, 11, 524. [Google Scholar] [CrossRef] [PubMed]
  57. Klein, C.S.; Marsh, G.D.; Petrella, R.J.; Rice, C.L. Muscle fiber number in the biceps brachii muscle of young and old men. Muscle Nerve 2003, 28, 62–68. [Google Scholar] [CrossRef]
  58. Anderson, G.S.; Gaetz, M.; Holzmann, M.; Twist, P. Comparison of EMG activity during stable and unstable push-up protocols. Eur. J. Sport Sci. 2013, 13, 42–48. [Google Scholar] [CrossRef]
  59. Czaprowski, D.; Stoliński, Ł.; Tyrakowski, M.; Kozinoga, M.; Kotwicki, T. Non-structural misalignments of body posture in the sagittal plane. Scoliosis Spinal Disord. 2018, 13, 6. [Google Scholar] [CrossRef] [Green Version]
  60. Houmard, J.A.; Weidner, M.L.; Gavigan, K.E.; Tyndall, G.L.; Hickey, M.S.; Alshami, A. Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J. Appl. Physiol. 1998, 85, 1337–1341. [Google Scholar] [CrossRef]
  61. Reinold, M.M.; Wilk, K.E.; Fleisig, G.S.; Zheng, N.; Barrentine, S.W.; Chmielewski, T.; Cody, R.C.; Jameson, G.G.; Andrews, J.R. Electromyographic Analysis of the Rotator Cuff and Deltoid Musculature During Common Shoulder External Rotation Exercises. J. Orthop. Sports Phys. Ther. 2004, 34, 385–394. [Google Scholar] [CrossRef] [Green Version]
  62. Lee, S.; Ooi, C. Evaluation of Achilles Tendon (AT) Stiffness: Comparison between Shearwave elastography and MyotonPro in Healthy AT. In Proceedings of the European Congress of Radiology-ESSR, Amsterdam, The Netherlands, 13–16 June 2018. [Google Scholar]
  63. Kawczyński, A.; Mroczek, D.; Andersen, R.E.; Stefaniak, T.; Arendt-Nielsen, L.; Madeleine, P. Trapezius viscoelastic properties are heterogeneously affected by eccentric exercise. J. Sci. Med. Sport 2018, 21, 864–869. [Google Scholar] [CrossRef]
  64. Xie, Y.; Thomas, L.; Hug, F.; Johnston, V.; Coombes, B.K. Quantifying cervical and axioscapular muscle stiffness using shear wave elastography. J. Electromyogr. Kinesiol. 2019, 48, 94–102. [Google Scholar] [CrossRef] [PubMed]
  65. Zhang, J.; Yu, J.; Liu, C.; Tang, C.; Zhang, Z. Modulation in Elastic Properties of Upper Trapezius with Varying Neck Angle. Appl. Bionics Biomech. 2019, 2019, 6048562. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Sokk, J.; Gapeyeva, H.; Ereline, J.; Merila, M.; Pääsuke, M. Shoulder muscle electromyographic activity and stiffness in patients with frozen shoulder syndrome: Six-month follow-up study. Acta Kinesiol. Univ. Tartu. 2013, 19, 73. [Google Scholar] [CrossRef] [Green Version]
  67. Roy, A.; Krebs, H.I.; Bever, C.T.; Forrester, L.W.; Macko, R.F.; Hogan, N. Measurement of passive ankle stiffness in subjects with chronic hemiparesis using a novel ankle robot. J. Neurophysiol. 2011, 105, 2132–2149. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Gordon, C.-M.; Andrasik, F.; Schleip, R.; Birbaumer, N.; Rea, M. Myofascial triggerpoint release (MTR) for treating chronic shoulder pain: A novel approach. J. Bodyw. Mov. Ther. 2016, 20, 614–622. [Google Scholar] [CrossRef]
  69. Vain, A.; Peipsi, A.; Mart, L. Device and Method for Real-Time Measurement of Parameters of Mechanical Stress State and Biomechanical Properties of Soft Biological Tissue (Patent No. US 2013/0289365 A1). Google Patent 2017. [Google Scholar]
  70. Hirata, K.; Kanehisa, H.; Miyamoto, N. Acute effect of static stretching on passive stiffness of the human gastrocnemius fascicle measured by ultrasound shear wave elastography. Eur. J. Appl. Physiol. 2017, 117, 493–499. [Google Scholar] [CrossRef]
  71. Wang, L.; Guo, X.; Tan, L.; Chen, Q. Quantitative assessment of normal middle deltoid muscle elasticity at various arm abduction using ultrasound shear wave elastography. Sci. Rep. 2021, 11, 112479. [Google Scholar] [CrossRef]
  72. Akagi, R.; Kusama, S. Comparison Between Neck and Shoulder Stiffness Determined by Shear Wave Ultrasound Elastography and a Muscle Hardness Meter. Ultrasound Med. Biol. 2015, 41, 2266–2271. [Google Scholar] [CrossRef]
  73. Sousa, A.S.P.; da Silva, C.I.C.; Mesquita, I.A.; Silva, A.; Macedo, R.; Imatz-Ojanguren, E. Optimal multi-field functional electrical stimulation parameters for the “drinking task—Reaching phase” and related upper limb kinematics repeatability in post stroke subjects. J. Hand Ther. 2021, 102, 1180–1190. [Google Scholar]
  74. Huang, J.; Qin, K.; Tang, C.; Zhu, Y.; Klein, C.S.; Zhang, Z.; Liu, C. Assessment of Passive Stiffness of Medial and Lateral Heads of Gastrocnemius Muscle, Achilles Tendon, and Plantar Fascia at Different Ankle and Knee Positions Using the MyotonPRO. Med Sci. Monit. 2018, 24, 7570–7576. [Google Scholar] [CrossRef]
  75. Lee, P.J.; Rogers, E.L.; Granata, K.P. Active trunk stiffness increases with co-contraction. J. Electromyogr. Kinesiol. Off. J. Int. Soc. Electrophysiol. Kinesiol. 2006, 16, 51–57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Mokkink, L.B.; Terwee, C.B.; Knol, D.L.; Stratford, P.W.; Alonso, J.; Patrick, D.L.; Bouter, L.M.; De Vet, H.C. The COSMIN checklist for evaluating the methodological quality of studies on measurement properties: A clarification of its content. BMC Med. Res. Methodol. 2010, 10, 22. [Google Scholar] [CrossRef] [Green Version]
  77. Kocur, P.; Wilski, M.; Lewandowski, J.; Łochyński, D. Female Office Workers with Moderate Neck Pain Have Increased Anterior Positioning of the Cervical Spine and Stiffness of Upper Trapezius Myofascial Tissue in Sitting Posture. PM&R 2019, 11, 476–482. [Google Scholar] [CrossRef]
  78. Park, S.J.; Kim, S.H.; Kim, S.H. Effects of Thoracic Mobilization and Extension Exercise on Thoracic Alignment and Shoulder Function in Patients with Subacromial Impingement Syndrome: A Randomized Controlled Pilot Study. Healthcare 2020, 8, 316. [Google Scholar] [CrossRef] [PubMed]
  79. Camargo, P.R.; Neumann, D.A. Kinesiologic considerations for targeting activation of scapulothoracic muscles—Part 2: Trapezius. Braz. J. Phys. Ther. 2019, 23, 467–475. [Google Scholar] [CrossRef]
  80. Ben Kibler, W.; McMullen, J.O.H.N.; Uhl, T.I.M. Shoulder rehabilitation strategies, guidelines, and practice. Orthop. Clin. N. Am. 2001, 32, 527–538. [Google Scholar] [CrossRef]
  81. Pizzari, T.; Wickham, J.; Balster, S.; Ganderton, C.; Watson, L. Modifying a shrug exercise can facilitate the upward rotator muscles of the scapula. Clin. Biomech. 2014, 29, 201–205. [Google Scholar] [CrossRef]
  82. Watson, L.; Pizzari, T.; Balster, S. Thoracic outlet syndrome Part 2: Conservative management of thoracic outlet. Man. Ther. 2010, 15, 305–314. [Google Scholar] [CrossRef]
  83. Castelein, B.; Cagnie, B.; Parlevliet, T.; Cools, A. Superficial and Deep Scapulothoracic Muscle Electromyographic Activity During Elevation Exercises in the Scapular Plane. J. Orthop. Sports Phys. Ther. 2016, 46, 184–193. [Google Scholar] [CrossRef]
  84. Ravichandran, H.; Janakiraman, B.; Gelaw, A.Y.; Fisseha, B.; Sundaram, S.; Sharma, H.R. Effect of scapular stabilization exercise program in patients with subacromial impingement syndrome: A systematic review. J. Exerc. Rehabil. 2020, 16, 216–226. [Google Scholar] [CrossRef]
  85. Navarro-Ledesma, S.; Fernandez-Sanchez, M.; Struyf, F.; Martinez-Calderon, J.; Morales-Asencio, J.M.; Luque-Suarez, A. Differences in scapular upward rotation, pectoralis minor and levator scapulae muscle length between the symptomatic, the contralateral asymptomatic shoulder and control subjects: A cross-sectional study in a Spanish primary care setting. BMJ Open 2019, 9, e023020. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Borstad, J.D. Measurement of Pectoralis Minor Muscle Length: Validation and Clinical Application. J. Orthop. Sports Phys. Ther. 2008, 38, 169–174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  87. Nogueira, N.; Oliveira-Campelo, N.; Lopes, Â.; Torres, R.; Sousa, A.S.P.; Ribeiro, F. The Acute Effects of Manual and Instrument-Assisted Cervical Spine Manipulation on Pressure Pain Threshold, Pressure Pain Perception, and Muscle-Related Variables in Asymptomatic Subjects: A Randomized Controlled Trial. J. Manip. Physiol. Ther. 2020, 43, 179–188. [Google Scholar] [CrossRef] [PubMed]
  88. Moon, J.-H.; Jung, J.-H.; Hahm, S.-C.; Oh, H.-K.; Jung, K.-S.; Cho, H.-Y. Effects of lumbar lordosis assistive support on craniovertebral angle and mechanical properties of the upper trapezius muscle in subjects with forward head posture. J. Phys. Ther. Sci. 2018, 30, 457–460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Kim, Y.; An, S.Y.; Park, W.; Hwang, J.H. Detection of early changes in the muscle properties of the pectoralis major in breast cancer patients treated with radiotherapy using a handheld myotonometer. Support. Care Cancer 2020, 29, 2581–2590. [Google Scholar] [CrossRef] [PubMed]
  90. Alizadeh, M.; Knapik, G.G.; Marras, W.S. Application of MR-derived cross-sectional guideline of cervical spine muscles to validate neck surface electromyography placement. J. Electromyogr. Kinesiol. 2018, 43, 127–139. [Google Scholar] [CrossRef]
  91. Johnson, G.; Bogduk, N.; Nowitzke, A.; House, D. Anatomy and actions of the trapezius muscle. Clin. Biomech. 1994, 9, 44–50. [Google Scholar] [CrossRef]
  92. Wallden, M. The trapezius—Clinical & conditioning controversies. J. Bodyw. Mov. Ther. 2014, 18, 282–291. [Google Scholar] [CrossRef]
  93. Ekstrom, R.A.; Bifulco, K.M.; Lopau, C.J.; Andersen, C.F.; Gough, J.R. Comparing the Function of the Upper and Lower Parts of the Serratus Anterior Muscle Using Surface Electromyography. J. Orthop. Sports Phys. Ther. 2004, 34, 235–243. [Google Scholar] [CrossRef] [Green Version]
  94. Park, S.-Y.; Yoo, W.-G. Differential activation of parts of the serratus anterior muscle during push-up variations on stable and unstable bases of support. J. Electromyogr. Kinesiol. 2011, 21, 861–867. [Google Scholar] [CrossRef]
  95. Smith, R., Jr.; Nyquist-Battie, C.; Clark, M.; Rains, J. Anatomical Characteristics of the Upper Serratus Anterior: Cadaver Dissection. J. Orthop. Sports Phys. Ther. 2003, 33, 449–454. [Google Scholar] [CrossRef] [PubMed]
  96. Tucker, W.S.; Campbell, B.M.; Swartz, E.E.; Armstrong, C.W. Electromyography of 3 Scapular Muscles: A Comparative Analysis of The Cuff Link Device and a Standard Push-Up. J. Athl. Train. 2008, 43, 464–469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Day, J.M.; Uhl, T. Thickness of the lower trapezius and serratus anterior using ultrasound imaging during a repeated arm lifting task. Man. Ther. 2013, 18, 588–593. [Google Scholar] [CrossRef]
  98. McKenna, L.J.; de Ronde, M.; Le, M.; Burke, W.; Graves, A.; Williams, S. Measurement of muscle thickness of the serratus anterior and lower trapezius using ultrasound imaging in competitive recreational adult swimmers, with and without current shoulder pain. J. Sci. Med. Sport 2018, 21, 129–133. [Google Scholar] [CrossRef]
  99. Owen, P.J.; Rantalainen, T.; Scheuring, R.A.; Belavy, D.L. Serratus Anterior Contraction During Resisted Arm Extension (GravityFit) Assessed by MRI. Front. Physiol. 2019, 10, 1164. [Google Scholar] [CrossRef] [PubMed]
  100. Salavati, M.; Akhbari, B.; Ebrahimi-Takamjani, I.; Ezzati, K.; Haghighatkhah, H. Reliability of the Upper Trapezius Muscle and Fascia Thickness and Strain Ratio Measures by Ultrasonography and Sonoelastography in Participants With Myofascial Pain Syndrome. J. Chiropr. Med. 2017, 16, 316–323. [Google Scholar] [CrossRef]
  101. Talbott, N.R.; Smith, A.M.; Stith, T.; Witt, D. Ultrasound Measurement of Levator Scapulae and Upper Trapezius Thickness during Scapular Elevation. In Proceedings of the 2020 APTA Combined Sections Meeting (CSM), Denver, CO, USA, 12–15 February 2020. [Google Scholar]
  102. Fujimoto, H.; Yabumoto, T.; Sugimori, H.; Shin, S.; Watanabe, T.; Matsuoka, T. Muscular Contraction Ability Develops in the Lower Trapezius Muscle of the Dominant Arm in Team Hand-Ball Players. Adv. Biosci. Biotechnol. 2015, 6, 368–374. [Google Scholar] [CrossRef] [Green Version]
  103. Hackett, L.; Reed, D.; Halaki, M.; Ginn, K.A. Assessing the validity of surface electromyography for recording muscle activation patterns from serratus anterior. J. Electromyogr. Kinesiol. 2014, 24, 221–227. [Google Scholar] [CrossRef]
  104. Sommerich, C.M.; Joines, S.; Hermans, V.; Moon, S.D. Use of surface electromyography to estimate neck muscle activity. J. Electromyogr. Kinesiol. 2000, 10, 377–398. [Google Scholar] [CrossRef]
  105. Ludewig, P.; Cook, T.M. The effect of head position on scapular orientation and muscle activity during shoulder elevation. J. Occup. Rehabil. 1996, 6, 147–158. [Google Scholar] [CrossRef]
  106. Choi, W.-J.; Cynn, H.-S.; Lee, C.-H.; Jeon, H.-S.; Lee, J.-H.; Jeong, H.-J.; Yoon, T.-L. Shrug exercises combined with shoulder abduction improve scapular upward rotator activity and scapular alignment in subjects with scapular downward rotation impairment. J. Electromyogr. Kinesiol. 2015, 25, 363–370. [Google Scholar] [CrossRef] [PubMed]
  107. Lee, J.-H.; Cynn, H.-S.; Choi, W.-J.; Jeong, H.-J.; Yoon, T.-L. Various shrug exercises can change scapular kinematics and scapular rotator muscle activities in subjects with scapular downward rotation syndrome. Hum. Mov. Sci. 2016, 45, 119–129. [Google Scholar] [CrossRef] [PubMed]
  108. Umehara, J.; Nakamura, M.; Nishishita, S.; Tanaka, H.; Kusano, K.; Ichihashi, N. Scapular kinematic alterations during arm elevation with decrease in pectoralis minor stiffness after stretching in healthy individuals. J. Shoulder Elb. Surg. 2018, 27, 1214–1220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  109. Umehara, J.; Nakamura, M.; Saeki, J.; Tanaka, H.; Yanase, K.; Fujita, K.; Yamagata, M.; Ichihashi, N. Acute and Prolonged Effects of Stretching on Shear Modulus of the Pectoralis Minor Muscle. J. Sports Sci. Med. 2021, 20, 17–25. [Google Scholar] [CrossRef] [PubMed]
  110. Castelein, B.; Cagnie, B.; Parlevliet, T.; Danneels, L.; Cools, A. Optimal Normalization Tests for Muscle Activation of the Levator Scapulae, Pectoralis Minor, and Rhomboid Major: An Electromyography Study Using Maximum Voluntary Isometric Contractions. Arch. Phys. Med. Rehabil. 2015, 96, 1820–1827. [Google Scholar] [CrossRef]
  111. Khosravi, F.; Rahnama, M.; Karimi, N.; Amiri, M.; Geil, M.D.; Rahnama, L. Rehabilitative ultrasound imaging of the levator scapula muscle at rest and during contraction: Technical description and reliability. J. Bodyw. Mov. Ther. 2021, 28, 411–417. [Google Scholar] [CrossRef]
  112. Cloke, D.J.; Watson, H.; Purdy, S.; Steen, I.N.; Williams, J.R. A pilot randomized, controlled trial of treatment for painful arc of the shoulder. J. Shoulder Elb. Surg. 2008, 17, S17–S21. [Google Scholar] [CrossRef]
  113. Hermans, J.; Luime, J.J.; Meuffels, D.E.; Reijman, M.; Simel, D.L.; Bierma-Zeinstra, S.M. Does this patient with shoulder pain have rotator cuff disease? The Rational Clinical Examination systematic review. JAMA 2013, 310, 837–847. [Google Scholar] [CrossRef]
  114. Ludewig, P.; Cook, T.M. Alterations in Shoulder Kinematics and Associated Muscle Activity in People with Symptoms of Shoulder Impingement. Phys. Ther. 2000, 80, 276–291. [Google Scholar] [CrossRef]
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Figure 1. Myotonometry tool and its specifications: a—Equipment, b—Coefficient of variation, c—Probe function, d—Measurement point, e—Adjacent tissue, f—Eligible muscles.
Figure 1. Myotonometry tool and its specifications: a—Equipment, b—Coefficient of variation, c—Probe function, d—Measurement point, e—Adjacent tissue, f—Eligible muscles.
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Figure 2. Graphical representation of the variables used in dynamic stiffness calculation.
Figure 2. Graphical representation of the variables used in dynamic stiffness calculation.
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Figure 3. Trapezius muscles assessment points: (a) upper trapezius C5/6 level; (b) upper trapezius C7 level; (c) middle trapezius; (d) lower trapezius.
Figure 3. Trapezius muscles assessment points: (a) upper trapezius C5/6 level; (b) upper trapezius C7 level; (c) middle trapezius; (d) lower trapezius.
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Figure 4. Upper trapezius muscles grid of measurement points.
Figure 4. Upper trapezius muscles grid of measurement points.
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Figure 5. Serratus anterior and levator assessment points: (e) levator scapulae; (f) SA upper/middle portion; (g) SA lower portion.
Figure 5. Serratus anterior and levator assessment points: (e) levator scapulae; (f) SA upper/middle portion; (g) SA lower portion.
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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).
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).
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Table
Table 1. Myotonometry validity data of correlation with shear wave elastography.
Table 1. Myotonometry validity data of correlation with shear wave elastography.
MuscleCorrelation Values
Values (p Value)Classification
Upper trapeziusr = −0.25 to 0.50 (p > 0.05) [1]Not statistically significant
Infraspinatusr = 0.35 to 0.37 (p < 0.05) [4]Fair
Rectus femorisr = 0.398 to 0.416 (p < 0.05 and p < 0.01, respectively) [56]
Biceps brachiir = 0.479 to 0.583 (p < 0.05) [49]Fair to Moderate
Gastrocnemiusr = 0.463 to 0.71 (p < 0.05 or p < 0.01) [4,18,56]Fair to Good
Erector spinaer = 0.51 to 0.54 (p < 0.05) [4]Moderate
Biceps femorisr = 0.594 to 0.652 (p < 0.01) [56]
Tibialis anteriorr = 0.540 to 0.561 (p < 0.01) [56]
Legend: Correlation values classification—no correlation if values <0.25, fair if 0.25–0.5, moderate to good if 0.5–0.75, and good to excellent if >0.75 [4].
Table
Table 2. Comparison between myotonometry and shear wave elastography for muscular stiffness assessment.
Table 2. Comparison between myotonometry and shear wave elastography for muscular stiffness assessment.
Shear Wave ElastographyMyotonometry
Instrument characteristics• Objective [4,18]
     • Non-invasive [1,4,18]
Real-time [1,3,64]
Required technical expertise [18]		Less expensive [1,4]
Handheld [1,3,4]
Easy to use [1,3,4,66]
Structures assessedDeep [1,4]Superficial [1,4]
Type of stiffness measuredPassive [1,3]: resistance to elongation or shortening or, in physical terms, the change in tension per unit change in length [67]Dynamic [1,25,68]: resistance to a force that deforms muscle initial shape [3,25,68]
Measurement modeElastic [4]/shear [3] modulus, that uses ultrasound radiation forces [4]Damped oscillation method following a dynamic transformation of the muscle in response to a short-term external mechanical impulse [69]
Measurement process
  • Transducer parallel to the muscle fibers [1,4,18]—wave travel horizontal (along fibers [15]) to the point of application through tissue [4]
  • Transducer held stationary for 10 s with minimal pressure applied on the skin [1,3,4]—acoustic radiation force to perturb muscle tissues [70]
  • Measurement estimate based on the velocity of ultrasound propagation from an entire defined region of interest [3,4,18] and based on tissue density [15]—converted into Kpa values through Young’s modulus formula for every pixel [3,71]
  • Probe perpendicular to the skin surface [1,3]
  • Constant pre-compression force (0.18 N) in the underlying tissues, followed by a short mechanical impulse (0.4/0.6 N for 15 ms) [1,4,18]
  • Recording of muscle oscillation [4], reflecting viscoelastic properties of the tissue [3]
  • Data by computational software, calculated from the acceleration of the testing probe during oscillations [3]
Measurement InterpretationVelocity of shear waves (proportional to shear modulus [64]) rise with increase in passive muscle stiffness [1,64]Higher values of dynamic stiffness imply more energy to modify the shape of the tissue [3]
Scapular muscles AssessedIn healthy subjects:In pain conditions:
  • UT [1,22];
  • Levator scapulae [22]
In healthy subjects:In pain conditions:
Results SWE vs. Myotonometry
  • Myotonometry presented lower coefficient of variability [4] and similar values of reliability compared to SWE
  • 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.
  • Myotonometry present ability to discriminate between different muscle contraction intensities, but the same did not happen always for SWE [4]
Legend: dynamic stiffness (DS); healthy subjects (HS); maximum amplitude of the acceleration of oscillation (amax); maximum displacement of the tissue (Δl); middle trapezius (MT); lower trapezius (LT); pain conditions (PC); probe mass (mprobe); shear wave elastography (SWE); upper trapezius (UT).
Table
Table 3. Myotonometry reliability data.
Table 3. Myotonometry reliability data.
MuscleSampleAssessment ConditionsReliability Values
Assessment MomentRaterMuscle ConditionICC ValuesClassification
Upper trapeziusHealthy and MSKdISInter-raterRest0.97 [7]Very high
HealthyISIntra-raterRest0.86 [48]High
BD0.229 [25] to 0.86 [63]Low to very high
ISInter-raterRest and contraction considered together0.97 [21]Very high
BDIntra-rater0.97 [21]Very high
Middle trapeziusBDIntra-raterRest0.813 to 0.963 [25]High to very high
Lower trapeziusBDIntra-raterRest0.820 to 0.926 [25]High to very high
InfraspinatusISIntra-raterRest0.98 [4]High to very high
Contraction0.98 [4]High to very high
Erector spinaeISIntra-raterRest1 [4]High to very high
Contraction0.99 to 1 [4]High to very high
Rectus femorisISIntra-raterRest0.938 [56]Very high
Contraction0.872 [56]High
Vastus LateralisISIntra-raterRest0.97 [3]Very high
BD0.93 [3]Very high
Medial gastrocnemiusISIntra-raterRest0.904 [56] to 1 [4]Very high
Contraction0.856 [56] to 0.99 [4]High to very high
Biceps femorisISIntra-raterRest0.884 [56]High
Contraction0.861 [56]High
Tibialis anteriorISIntra-raterRest0.880 [56]High
Contraction0.894 [56]High
Legend: BD: between days; IS: intrasession; MSKd: musculoskeletal disorders; Reliability values classification—little, if any reliability, if values <0.15, low if 0.16–0.49, moderate if 0.50–0.69, high if 0.70–0.89, and very high if values >0.90 [73].
Table
Table 4. Description of the trapezius muscle assessment points.
Table 4. Description of the trapezius muscle assessment points.
Muscle of InterestMeasurement Points
Upper trapezius C5/6 levelAt the level of C5/C6 about 2 cm lateral from the midline [90]
Upper trapezius C7 levelMid-way between C7 spinous process and the angle of acromion [7,12,21,87,88,89]
Middle trapeziusMid-way from T4 spinous process to the medial border of spine of the scapulae [25]
Lower TrapeziusMid-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]
Table
Table 5. Description of the serratus anterior and levator scapulae assessment points.
Table 5. Description of the serratus anterior and levator scapulae assessment points.
Muscle of InterestMeasurement Points
Levator scapulaeBetween 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 portionOver the fourth rib, at the midpoint between the latissimus dorsi and the pectoralis major [93,94]
SA lower portionOver the seventh rib, in the midline of the axilla [93], for SA lower portion (SAlow) [93]
Table
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.
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.
Study ObjectiveGroupMuscle Assessed X ¯ SD (N/m)p Value
Mild (until 3 in VAS) UT pain (20.83 ± 1.12 years old) [26]BGc✓VAS 0UT
(muscle belly)		170.5628.45p < 0.05 *,
for VAS 3 in comparison with other 3 groups
VAS 1161.6716.59
VAS 2160.4820.72
VAS 3191.5025.74
IE--
Moderate work-related neck
disorders
(30–55 years old) [77]		BGc✓PainUT
(C5/6 and C7 level)		301.5023.50p = 0.006 *
Control270.9033.70
IE--
Unilateral chronic
shoulder pain together with, at least, 2 sensitive sites (myofascial trigger points)
(18–70 years old) [68]		BGcXControl (Us, before)UT
(trigger points)		324.4211.39p = 0.057
Control (Us, after)334.6811.10
Pain (before)332.3210.97
Pain (after)300.669.43
IE✓
for
Myofascial trigger-point
Release		Pain (before vs. after)p = 0.012 *
Long-standing, nonspecific and nontraumatic neck-shoulder pain
(20–61 years old) [14]		BGcXControl (MB sites)UT
(15 adjacent points)		237.8042.8p = 0.273,
for
comparison of both measurement sites
Control (Mt sites)327.5055.9
Pain (MB sites before)258.7041.10
Pain (Mt sites before)330.4050.8
IE✓
for
Eccentric
Training		Pain (MB sites after)226.8020.00p < 0.001 *,
for comparison in both measurement sites
Pain (Mt sites after)287.3047.80
Subacromial
impingement syndrome (49.20 ± 9.48 to 50.90 ± 9.10 years old) [78]		BGc--
IE✓
for Thoracic
mobilization and/or
Extension exercise		Pain (TM before)UT
(center of muscle belly)		257.9029.03p = 0.001 *
Pain (TM after)232.5020.49
Pain (exercise before)257.7019.33p = 0.001 *
Pain (exercise after)236.1027.27
Pain (TM plus exercise before)257.5025.61p = 0.001 *
Pain (TM plus exercise after)223.0032.83
Stage II or III of unilateral frozen shoulder
syndrome
(38–74 years old) [66]		BGcXControl (Us, before)UT
(center of muscle belly)		≈235_p > 0.05
Control (Us, 1 m after)≈215_
Control (Us, 6 m after)≈200_
Pain (before)≈240_
Pain (1 m after)≈225_
Pain (6 m after)≈220_
IEX
for Manual
manipulation (under anaesthesia)		Pain (before vs. after)p > 0.05, for comparison in each assessment moments
Unilateral neck or shoulder pain and active myofascial trigger points in the
trapezius
muscle
(19.8 ± 2.4 years old) [25]		BGc--
IE✓
for Ischemic
compression		PainUT
(distally of muscle belly’s center)		232.0029.70p = 0.03 *
UT2
(proximally of muscle belly’s center)		269.0042.10
MT405.30192.10p = 0.40
LT
(mid-point)		347.50110.40p = 0.29
LT
(lateral border mid-point of muscle fibers)		331.7089.30
Legend: ≈: when stiffness values were only presented in the original study through a graphic; 1 m: one month; 6 m: six months; After: stiffness values measured after intervention; Before: stiffness values measured before intervention; BGc: between groups comparison; IE: Intervention effects (comparison between pre and post-intervention moments); LT: lower trapezius; MB: muscle belly sites; Mt: myotendinous sites; MT: middle trapezius; SD: standard deviation; TM: thoracic mobilization; Us: unaffected side; UT: upper trapezius; VAS: visual analog scale; X ¯ : mean.
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Melo, A.S.C.; Cruz, E.B.; Vilas-Boas, J.P.; Sousa, A.S.P. Scapular Dynamic Muscular Stiffness Assessed through Myotonometry: A Narrative Review. Sensors 2022, 22, 2565. https://doi.org/10.3390/s22072565

AMA Style

Melo ASC, Cruz EB, Vilas-Boas JP, Sousa ASP. Scapular Dynamic Muscular Stiffness Assessed through Myotonometry: A Narrative Review. Sensors. 2022; 22(7):2565. https://doi.org/10.3390/s22072565

Chicago/Turabian Style

Melo, Ana S. C., Eduardo B. Cruz, João Paulo Vilas-Boas, and Andreia S. P. Sousa. 2022. "Scapular Dynamic Muscular Stiffness Assessed through Myotonometry: A Narrative Review" Sensors 22, no. 7: 2565. https://doi.org/10.3390/s22072565

APA Style

Melo, A. S. C., Cruz, E. B., Vilas-Boas, J. P., & Sousa, A. S. P. (2022). Scapular Dynamic Muscular Stiffness Assessed through Myotonometry: A Narrative Review. Sensors, 22(7), 2565. https://doi.org/10.3390/s22072565

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