- Email: [email protected]
Assessment of the Passive Tension of the First Dorsal Interosseous and First Lumbrical Muscles Using Shear Wave Elastography
SCIENTIFIC ARTICLE
Assessment of the Passive Tension of the First Dorsal Interosseous and First Lumbrical Muscles Using Shear Wave Elastography Yudai Watanabe, PhD,*‡ Kousuke Iba, MD, PhD,* Keigo Taniguchi, PhD,§ Mitsuhiro Aoki, MD, PhD,k Tomoko Sonoda, PhD,† Toshihiko Yamashita, MD, PhD* Purpose Quantitative evaluation of passive tension of the intrinsic muscles of the hand is necessary to assess contracture of the intrinsic muscles accurately. The aim of this study was to evaluate the shear modulus, which is related to passive muscle tension, of the first dorsal interosseous (FDI) and first lumbrical (FL) muscles using shear wave elastography. Methods Subjects were 18 healthy males. The shear modulus of the FDI and FL muscles was assessed at several proximal interphalangeal (PIP), distal interphalangeal (DIP), metacarpophalangeal (MCP), and wrist joint positions. The position in which the MCP joint was flexed 60 past 0 with PIP-DIP joint extension and that in which the MCP joint was extended 30 past 0 with PIP-DIP joint flexion were respectively defined as the slack and stretched positions. We analyzed whether the shear modulus was affected by finger position (slack or stretched), wrist position (30 flexion past 0 and 30 extension past 0 ), and muscle (FDI or FL). Results Shear modulus in the stretched position was significantly higher than that in the slack position. The shear modulus of the FL muscle at 30 wrist extension was significantly higher than that at 30 flexion. The shear modulus of the FL muscle was significantly higher than that of the FDI muscle in the stretched position with the wrist at 30 flexion and extension, and in the slack position with the wrist at 30 extension. Conclusions The shear modulus of the FDI and FL muscles increased with MCP joint extension and PIP-DIP joint flexion. The difference in the muscle characteristics between the FDI and FL muscles should be considered when evaluating or treating contractures of the intrinsic muscles. Clinical relevance Shear wave elastography can evaluate the condition of the intrinsic muscles of the hand quantitatively. (J Hand Surg Am. 2019;-(-):1.e1-e8. Copyright Ó 2019 by the American Society for Surgery of the Hand. All rights reserved.) Key words hand intrinsic muscles, passive muscle tension, shear wave elastography.
T
HE INTRINSIC MUSCLES OF THE hand have an essential role in hand dexterity. The interosseous and lumbrical muscles originate from the metacarpals and flexor digitorum profundus
(FDP) tendons, respectively, and the tendons of these muscles comprise the lateral band, which inserts dorsally to the extensor apparatus. The intrinsic muscles function in metacarpophalangeal (MCP)
From the *Department of Orthopaedic Surgery and †Department of Public Health, Sapporo Medical University School of Medicine; the ‡Division of Rehabilitation, Sapporo Medical University Hospital; and the §Second Division of Physical Therapy, Sapporo Medical University School of Health Sciences, Sapporo; and the kDepartment of Physical Therapy, School of Rehabilitation Sciences, Health Science University of Hokkaido, Ishikari, Hokkaido, Japan.
No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.
Received for publication April 8, 2018; accepted in revised form January 14, 2019.
0363-5023/19/---0001$36.00/0 https://doi.org/10.1016/j.jhsa.2019.01.016
Corresponding author: Yudai Watanabe, PhD, Department of Orthopaedic Surgery, Sapporo Medical University School of Medicine, South 1, West 16, Chuo-ku, Sapporo, Hokkaido 060-8543, Japan; e-mail: [email protected].
Ó 2019 ASSH
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joint flexion and proximal interphalangeal (PIP)e distal interphalangeal (DIP) joint extension, and also contribute to grip and pinch strength.1 Several studies have indicated that strengthening and stretching of the intrinsic muscles may lead to improved hand dexterity, better fatigue endurance, and improved range of motion (ROM).2e4 Contracture of the intrinsic muscles causes severe impairment of hand function by generating an intrinsic-plus hand and swan neck deformities.5e7 Even in cases of mild contracture, patients may report tightness on PIP-DIP joint flexion with MCP joint extension and impaired hand dexterity.7 This contracture has been qualitatively evaluated by the intrinsic tightness test. In this test, when flexion of the PIP joint is limited with MCP joint extension, intrinsic tightness is present.5e9 Contracture of the intrinsic muscles has been treated by stretching exercises that emphasize MCP joint extension with PIPDIP joint flexion.8,9 However, qualitative methods are insufficient to evaluate the severity of contracture or the therapeutic effect of stretching exercises. Therefore, a quantitative evaluation method is needed that measures the passive muscle tension of the intrinsic muscles. Passive muscle stiffness has been estimated by the slope of forceemuscle length curve, based on the relation of joint angle and passive joint torque or displacement of the myotendinous junction using ultrasonography.10e12 However, these methods indirectly calculate the tension as a relative value. Recently, shear wave elastography has been used to assess the stiffness of soft tissue as the shear modulus without measuring the slope of the stressestrain curve. This apparatus uses transient and remote mechanical vibration generated by an acoustic radiation force at a localized area. The force causes tissue dislocation and generates a shear wave. Then, the apparatus calculates the shear modulus from the propagation of shear wave speed.13 In terms of muscle tissue, Maïsetti et al14 reported that the relation between the shear modulus and muscle length was highly correlated with the forceemuscle length curve. Moreover, Koo et al15 reported that the shear modulus was related to muscle force during passive stretching ex vivo. These studies indicated that passive muscle tension could be measured directly as an absolute value by shear wave elastography.16e22 We sought to evaluate the passive tension of the intrinsic muscles using this method, and to confirm tension with the muscle in a slack and stretched position. The specific aims of this study were to assess shear modulus in first dorsal interosseous (FDI) and first J Hand Surg Am.
lumbrical (FL) muscles in several MCP and PIP-DIP joint positions. In addition, we examined whether wrist position affected the shear modulus of the intrinsic muscles, because the lumbrical muscles originate from the FDP tendon, which changes tension according to wrist position. MATERIALS AND METHODS Subjects Subjects consisted of 18 healthy male volunteers (aged 30.9 4.3 years; range, 25e40 years). We excluded subjects from this study owing to (1) any abnormality of the right upper limb resulting from trauma, degenerative disease, or disorders of the central or peripheral nervous systems; and (2) hypermobility of the MCP joint of the index finger for which passive extension was more than 90 . The purpose and procedures of the study were explained to all subjects before participation. This study was approved by the ethics board of Sapporo Medical University. Protocols Subjects were placed in a sitting position with the shoulder at 0 adduction and the elbow at 90 flexion. To assess the shear modulus of the FDI and FL muscles, the forearm was pronated and supinated, respectively. The forearm was placed on a custom-made jig that could adjust the angle of the wrist joint and the MCP joint of the index finger. The forearm and fingers were immobilized with an orthosis and hook-and-loop fasteners. The PIP-DIP joint was set in 2 positions (full flexion and full extension) and the MCP joint in 4 positions (60 , 30 and 0 flexion past neutral, and 30 extension past 0 ). Shear modulus with the MCP joint at 60 flexion with PIP-DIP joint flexion could not be measured owing to the lack of space to position the probe. The position in which the MCP joint was at 60 flexion with PIP-DIP joint extension was defined as the slack position (Figs. 1A, 2A), and that in which the MCP joint was at 30 extension with PIP-DIP joint flexion was defined as the stretched position (Figs. 1G, 2G). There were 7 combinations of finger position (Figs. 1, 2) and the wrist position was set in 3 positions (30 flexion past 0 , neutral, and 30 extension past 0 ). In total, shear modulus was measured for 42 combinations (7 finger positions 3 wrist positions 2 muscles). The measurement order for the 6 positions (3 wrist positions 2 muscles) and 7 finger positions was randomized in advance. r
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FIGURE 1: Finger position for measurement of shear modulus of FDI muscle. A Metacarpophalangeal joint at 60 flexion with PIP-DIP joint extension. B Metacarpophalangeal joint at 30 flexion with PIP-DIP joint extension. C Metacarpophalangeal joint at 0 flexion with PIP-DIP joint extension. D Metacarpophalangeal joint at 30 extension with PIP-DIP joint extension. E Metacarpophalangeal joint at 30 flexion with PIP-DIP joint flexion. F Metacarpophalangeal joint at 0 flexion with PIP-DIP joint flexion. G Metacarpophalangeal joint at 30 extension with PIP-DIP joint flexion. (A) and (G) were defined as slack and stretched positions, respectively.
Shear modulus Shear modulus was measured by ultrasound shear wave elastography (version 4, AixPlorer, SuperSonic Imagine, Aix-en-Provence, France) with a linear array probe (50 mm, 4e15 MHz). The probe was applied to the dorsal and palmar hand to image the FDI and FL muscles, respectively, with acoustic gel (Fig. 3). The examiner manually operated the probe to maintain the shape of FDI and FL muscles. In anisotropic tissue such as muscle tissue, measurement of shear modulus changes by the position of the probe relative to the direction of the muscle fiber; it is recommended that it be measured in a longitudinal direction.23,24 The probe was set longitudinally along the direction of the muscle to observe the area of maximum muscle thickness. We analyzed ultrasonographic images of the FDI and FL muscles in accordance with the method reported by Infantolino et al25 and Jacobson26 (Fig. 4). The ultrasound device generated shear waves via the probe into the soft tissue and detected the shear wave propagation speed (c, m/s). Young’s modulus (E) was then calculated by the device as:
J Hand Surg Am.
E ¼ 3pc2
where p is the tissue density, which was assumed to be a constant 1,000 kg/m3 for human soft tissue.27 Young’s modulus was quantified based on an assumption of isotropic tissue; however, skeletal muscle cannot be assumed to be isotropic. In anisotropic tissue, measurement using the shear modulus rather than Young’s modulus is recommended.28 The shear modulus (G) was calculated as: G ¼ E = 2ð1 þ vÞ
where v is Poisson’s ratio, which is close to 0.5 for tissue assumed to be incompressible, such as skeletal muscle.19 Hence, we adopted the shear modulus as the value obtained by dividing Young’s modulus by 3. Young’s modulus was presented as a color-coded 15 15-mm2 region of interest (ROI) over a Bmode image. Within the ROI, a circular area was selected and the average Young’s modulus (in
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FIGURE 2: Finger positions for measurement of shear modulus of FL muscle. A Metacarpophalangeal joint at 60 flexion with PIP-DIP joint extension. B Metacarpophalangeal joint at 30 flexion with PIP-DIP joint extension. C Metacarpophalangeal joint at 0 flexion with PIP-DIP joint extension. D Metacarpophalangeal joint at 30 extension with PIP-DIP joint extension. E Metacarpophalangeal joint at 30 flexion with PIP-DIP joint flexion. F Metacarpophalangeal joint at 0 flexion with PIP-DIP joint flexion. G Metacarpophalangeal joint at 30 extension with PIP-DIP joint flexion. (A) and (G) were defined as slack and stretched positions, respectively.
kilopascals) was calculated for this area. The diameter of the circular area was set from 2 to 5 mm, depending on muscle thickness; the number of circles was set from 3 to 6 according to the ROI. The measurement value was derived from the average of the number of circular areas. We used the mean value of 2 measurements for statistical analysis.
positions. The root mean square of the EMG (RMSEMG) data was calculated for 100 milliseconds. The RMS-EMG was then calculated as the percentage of MVC (%MVC). The %MVC for the FL muscle was calculated using the same procedure. Range of motion Maximum passive ROM of the MCP joint with PIPDIP joint flexion or extension was measured after EMG was assessed.
Electromyography We confirmed that muscle activity had no effect on the measurement of the shear modulus using EMG. Surface EMG was measured after shear modulus measurement as follows: After the skin was cleaned with alcohol, the electrode (size: 1 6 mm; interelectrode distance: 12 mm; DL-141, S&ME, Tokyo, Japan) was placed in the same position as the probe. A reference electrode was placed over the styloid process of the ulna. The EMG data was simultaneously recorded using software (Labchart 7 Pro, AD Instruments, Sydney, Australia) via an analog-todigital converter (PowerLab 16/30, AD Instruments). After we measured the maximum voluntary contraction (MVC) of the FDI muscle, we recorded EMG data for the FDI muscle for 20 seconds in the 21 J Hand Surg Am.
Statistics For statistical analysis of the shear modulus data, we used 3-way analysis of variance with repeated measures for the finger position (slack and stretched), wrist position (30 flexion and 30 extension), and muscle (FDI and FL) with significance set at .05. A paired t test was performed for pairwise comparisons as a post hoc test. The Bonferroni correction with a significance level of .05 / 4 ¼ .0125 was applied. Measurement reliability between the first and second measurements for the 42 combinations was assessed using the intraclass correlation coefficient (ICC). r
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with the wrist at 30 flexion with the slack position was significantly higher than that with the wrist at 30 extension with the slack position (P ¼ .007). There was no significant difference between values obtained for the FDI muscle in the wrist at 30 flexion and extension with the stretched position (P ¼ .715). Shear modulus of the FL muscle was significantly higher than that of the FDI muscle with the wrist at 30 flexion (P ¼ .001) (Fig. 6B) and extension (P < .001) with the stretched position, and with the wrist at 30 extension with the slack position (P ¼ .001). There was no significant difference between values obtained for the FL and FDI muscles with the wrist at 30 flexion in the slack position (P ¼ .550). The ICC between the first and second measurements for the 42 combinations ranged from 0.808 to 0.988. In addition, all %MVC data were less than 3.2% and mean values for the FDI and FL muscles ranged from 0.71% to 1% and from 1.16% to 1.57%, respectively.
FIGURE 3: Measurement method for the shear modulus of FL and FDI muscles by ultrasound shear wave elastography. The forearm was placed on a custom-made jig that allowed adjustment of the angle of the wrist and MCP joint of the index finger. The forearm and fingers were immobilized with an orthosis and hook-and-loop fasteners. The linear array probe was applied to the dorsal and palmar hand to image the A FDI and B FL muscles, respectively, with acoustic gel.
DISCUSSION We evaluated passive tension of the FDI and FL muscles quantitatively by measuring the shear modulus value at various finger and wrist joint positions. In particular, we found that the shear modulus for the FDI and FL muscles increased with MCP joint extension and PIP-DIP joint flexion. This result indicated that the intrinsic tightness test and the manner in which this position is used for stretching exercises for the intrinsic muscles are valuable for assessing and treating intrinsic muscles contracture. The shear modulus of FL muscle was higher than that of the FDI muscle in the stretching position. This result suggests that the intrinsic tightness test is likely to reflect lumbrical muscle more than interosseous muscle tightness. In addition, contracture of the lumbrical muscle would be discriminated by the wrist position because the shear modulus of the FL muscle became higher with wrist extension. Therefore, we think that this quantitative evaluation would be useful for analyzing the intrinsic tightness test more accurately. Interestingly, the shear modulus of the FL muscle increased significantly with wrist and MCP joint extension. A possible explanation for this is that the shear modulus of the FL was affected by tension in the FDP tendon, which is the origin of the lumbrical muscles. Tension in the FDP tendon increases with MCP and wrist joint extension,29 and this might be transmitted to the shear modulus of the lumbrical muscle. In addition, the shear modulus of the FDI
RESULTS Three subjects were excluded from the original pool of 21 because stable color-coded maps for the FL muscle in 2 subjects and a clear B-mode image of the FL muscle in 1 could not be measured. We obtained complete data for 18 of the 21 subjects. Maximum passive flexion angle of the MCP joint with PIP-DIP joint flexion and extension was 89.7 8.3 and 93.1 8.9 , respectively. Maximum passive extension angle of the MCP joint with PIP-DIP joint flexion and extension was 56.4 8.4 and 60.6 7.6 , respectively. Minimum and maximum shear modulus values for the FDI and FL muscles were obtained in the slack and stretched positions, respectively, regardless of wrist position (Fig. 5). There were significant interactions in the shear modulus value among finger position, wrist position, and muscle (P < .001; 3-way analysis of variance). The shear modulus in the stretched position (MCP joint at 30 extension with PIP-DIP flexion) was significantly higher than that in the slack position (MCP joint at 60 flexion with PIP-DIP extension) independent of wrist position and muscle (P < .001). Shear modulus of the FL muscle in the wrist at 30 extension was significantly higher than that at 30 flexion with both the slack and stretched positions (P .001) (Fig. 6A). Shear modulus of the FDI muscle J Hand Surg Am.
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FIGURE 4: Ultrasonographic findings for FDI and FL muscles. A The FDI muscle was identified as the muscle tissue above the FDI tendon originating from the second metacarpal head. The color-coded region of interest (ROI) indicates the shear modulus. The average of Young’s modulus was calculated for circular area within the ROI. The ROI was set at areas with the maximum observable muscle thickness. B The FL muscle was identified at the same depth as the flexor tendon. The right end of the ROI was set in the same position as the right end of the adductor pollicis muscle.
FIGURE 5: Shear modulus of FDI and FL muscles at various finger and wrist positions. A Shear modulus of the FDI muscle. B Shear modulus of the FL muscle. The minimum shear modulus value was obtained with the MCP joint at 60 flexion with PIP-DIP joint extension in all wrist positions. The maximum shear modulus value was obtained with the MCP joint at 30 extension with PIP-DIP joint flexion in all wrist positions. PIPDIPExt, PIP-DIP joint extension; PIPDIPFlex, PIP-DIP joint flexion; WE, wrist at 30 extension; WF, wrist at 30 flexion; WN, wrist in neutral position.
muscle in the slack position slightly but significantly increased with wrist flexion. The interosseous muscles insert into the extensor digitorum communis tendon, and tension in that tendon, which is increased by MCP joint and wrist flexion, could be transmitted to the interosseous muscles. Thus, the shear modulus of the FDI and FL muscles is affected by wrist position. These results indicate that the wrist position should be taken into consideration when assessing contracture of the intrinsic muscles. Moreover, we recommend that wrist position be fixed when measuring the shear modulus of the FDI and FL muscles by shear wave elastography.
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Shear modulus of the FL muscle in the stretched position was higher than that of the FDI muscle. Koo and Hug30 suggested that the shear modulus was primarily affected by the muscle cross-sectional area, with which it was negatively correlated. Jacobson et al31 reported that the cross-sectional area of the FDI and FL muscles was 1.50 and 0.11 cm2, respectively, which corresponded to the results of their study. Hirata et al32 suggested that stretching notably affects muscles with the highest shear modulus value. Based on these and our studies, stretching exercises might have a more marked effect on the FL muscle than on the FDI muscle.
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FIGURE 6: Post hoc analysis after 3-way analysis of variance for the shear modulus values for the FDI and FL muscles. A Comparison of the shear modulus between 30 flexion and 30 extension of the wrist. B Comparison of the shear modulus between the FDI and FL muscles. FSL, finger slack position; FST, finger stretched position; WE, wrist at 30 extension; WF, wrist at 30 flexion. *P < .0125.
Recently, several studies20e22,32,33 indicated a decrease in the shear modulus after stretching exercises in healthy subjects, and those changes depended on the different rehabilitation programs. In treating intrinsic muscles contracture, it is important to compare clinical status before and after treatment. Further study is required to evaluate the therapeutic effect from the viewpoint of the shear modulus of intrinsic muscles. We separately assessed the shear modulus and EMG of the FDI and FL muscles, the size of which was too small to position the probe and the EMG recorder simultaneously. It is controversial whether the threshold of EMG activity (%MVC) of a muscle could affect the shear modulus. In this study, the change in %MVC of the FDI and FL muscles was only 0.29% and 0.41%, respectively, during passive joint movement. These results indicated that EMG activity has little effect on the shear modulus. We conclude that the current data are reliable and accurate. There were several limitations to this study. First, the shear modulus of the FL muscle could not be assessed in 3 subjects. This was probably because of the thickness of the skin or the existence of palmar fascia. Second, this study demonstrated the shear modulus of only the FDI and FL muscles. The other intrinsic muscles of the hand would not necessarily have had identical results. Third, we could not constantly set the probe in the same position. Miyamoto et al34 reported that the difference in the shear modulus value was negligible when the probe is positioned parallel to the fascicle and at 20 oblique to the fascicle, whereas Maïsetti et al14 indicated that an increase in probe rotation affected accurate measurement of the shear modulus. In the current study, the ICC between the first and second measurements J Hand Surg Am.
was greater than 0.8. We conclude that setting the probe by hand has little influence on measurements of the shear modulus. We measured the shear modulus of the FDI and FL muscles by shear wave elastography in various positions of the PIP-DIP, MCP, and wrist joints. The shear modulus of each muscle increased with MCP joint extension and PIP-DIP joint flexion. The shear modulus of each muscle was also affected by wrist position. We found that passive tension of the FL muscle was higher than that of the FDI muscle. The results of our study suggest that quantitative evaluation using shear wave elastography could allow more accurate evaluation of the severity of contracture and of the therapeutic effect of stretching. REFERENCES 1. Kozin SH, Porter S, Clark P, Thoder JJ. The contribution of the intrinsic muscles to grip and pinch strength. J Hand Surg Am. 1999;24(1):64e72. 2. Less M, Krewer SE, Eickelberg WW. Exercise effect on strength and range of motion of hand intrinsic muscles and joints. Arch Phys Med Rehabil. 1977;58(8):370e374. 3. Penn IW, Chuang TY, Chan RC, Hsu TC. EMG power spectrum analysis of first dorsal interosseous muscle in pianists. Med Sci Sports Exerc. 1999;31(12):1834e1838. 4. Olafsdottir HB, Zatsiorsky VM, Latash ML. The effects of strength training on finger strength and hand dexterity in healthy elderly individuals. J Appl Physiol (1985). 2008;105(4):1166e1178. 5. Finochietto R. Retracción de Volkmann de los músculos intrínsecos de la mano. Bol Trab Soc Cir B Aires. 1920;4:31e37. 6. Bunnell S, Doherty EW, Curtis RM. Ischemic contracture, local, in the hand. Plast Reconstr Surg (1946). 1948;3(4):424e433. 7. Tosti R, Thoder JJ, Ilyas AM. Intrinsic contracture of the hand: diagnosis and management. J Am Acad Orthop Surg. 2013;21(10): 581e591. 8. McEntee PM. Therapist’s management of the stiff hand. In: Hunter JM, Schneider LH, Mackin EJ, Callahan AD, eds. Rehabilitation of the Hand: Surgery and Therapy. 3rd ed. St. Louis, MO: Mosby; 1990:328e341. 9. Seu M, Pasqualetto M. Hand therapy for dysfunction of the intrinsic muscles. Hand Clin. 2012;28(1):87e100.
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22. Miyamoto N, Hirata K, Kanehisa H. Effects of hamstring stretching on passive muscle stiffness vary between hip flexion and knee extension maneuvers. Scand J Med Sci Sports. 2017;27(1):99e106. 23. Gennisson JL, Deffieux T, Macé E, Montaldo G, Fink M, Tanter M. Viscoelastic and anisotropic mechanical properties of in vivo muscle tissue assessed by supersonic shear imaging. Ultrasound Med Biol. 2010;36(5):789e801. 24. Alfuraih AM, O’Connor P, Tan AL, Hensor E, Emery P, Wakefield RJ. An investigation into the variability between different shear wave elastography systems in muscle. Med Ultrason. 2017;19(4):392e400. 25. Infantolino BW, Challis JH. Measuring subject specific muscle model parameters of the first dorsal interosseous in vivo. Ann Biomed Eng. 2014;42(6):1331e1339. 26. Jacobson JA. Fundamentals of Musculoskeletal Ultrasound. Philadelphia, PA: Saunders; 2007. 27. Gennisson JL, Cornu C, Catheline S, Fink M, Portero P. Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech. 2005;38(7):1543e1550. 28. Royer D, Gennisson JL, Deffieux T, Tanter M. On the elasticity of transverse isotropic soft tissues (L). J Acoust Soc Am. 2011;129(5): 2757e2760. 29. Tanaka T, Amadio PC, Zhao C, Zobitz ME, An KN. Flexor digitorum profundus tendon tension during finger manipulation. J Hand Ther. 2005;18(3):330e338. 30. Koo TK, Hug F. Factors that influence muscle shear modulus during passive stretch. J Biomech. 2015;48(12):3539e3542. 31. Jacobson MD, Raab R, Fazeli BM, et al. Architectural design of the human intrinsic hand muscles. J Hand Surg Am. 1992;17(5):804e809. 32. Hirata K, Miyamoto-Mikami E, Kanehisa H, Miyamoto N. Musclespecific acute changes in passive stiffness of human triceps surae after stretching. Eur J Appl Physiol. 2016;116(5):911e918. 33. Yamauchi T, Hasegawa S, Nakamura M, et al. Effects of two stretching methods on shoulder range of motion and muscle stiffness in baseball players with posterior shoulder tightness: a randomized controlled trial. J Shoulder Elbow Surg. 2016;25(9):1395e1403. 34. Miyamoto N, Hirata K, Kanehisa H, Yoshitake Y. Validity of measurement of shear modulus by ultrasound shear wave elastography in human pennate muscle. PLoS One. 2015;10:e0124311.
10. Toft E, Espersen GT, Kålund S, Sinkjaer T, Hornemann BC. Passive tension of the ankle before and after stretching. Am J Sports Med. 1989;17(4):489e494. 11. Morse CI, Degens H, Seynnes OR, Maganaris CN, Jones DA. The acute effect of stretching on the passive stiffness of the human gastrocnemius muscle tendon unit. J Physiol. 2008;586(1):97e106. 12. Hwang W, Kelly NG, Boriek AM. Passive mechanics of muscle tendinous junction of canine diaphragm. J Appl Physiol (1985). 2005;98(4):1328e1333. 13. Nowicki A, Dobruch-Sobczak K. Introduction to ultrasound elastography. J Ultrason. 2016;16(65):113e124. 14. 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(6): 978e984. 15. Koo TK, Guo JY, Cohen JH, Parker KJ. Relationship between shear elastic modulus and passive muscle force: an ex-vivo study. J Biomech. 2013;46(12):2053e2059. 16. Hirata K, Kanehisa H, Miyamoto-Mikami E, Miyamoto N. Evidence for intermuscle difference in slack angle in human triceps surae. J Biomech. 2015;48(6):1210e1213. 17. Lacourpaille L, Hug F, Nordez A. Influence of passive muscle tension on electromechanical delay in humans. PLoS One. 2013;8: e53159. 18. Koo TK, Guo JY, Cohen JH, Parker KJ. Quantifying the passive stretching response of human tibialis anterior muscle using shear wave elastography. Clin Biomech (Bristol, Avon). 2014;29(1):33e39. 19. Eby SF, Cloud BA, Brandenburg JE, et al. Shear wave elastography of passive skeletal muscle stiffness: influences of sex and age throughout adulthood. Clin Biomech (Bristol, Avon). 2015;30(1): 22e27. 20. Taniguchi K, Shinohara M, Nozaki S, Katayose M. Acute decrease in the stiffness of resting muscle belly due to static stretching. Scand J Med Sci Sports. 2015;25(1):32e40. 21. Andrade RJ, Lacourpaille L, Freitas SR, McNair PJ, Nordez A. Effects of hip and head position on ankle range of motion, ankle passive torque, and passive gastrocnemius tension. Scand J Med Sci Sports. 2016;26(1):41e47.
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Assessment of the Passive Tension of the First Dorsal Interosseous and First Lumbrical Muscles Using Shear Wave Elastography Yudai Watanabe, PhD,*‡ Kousuke Iba, MD, PhD,* Keigo Taniguchi, PhD,§ Mitsuhiro Aoki, MD, PhD,k Tomoko Sonoda, PhD,† Toshihiko Yamashita, MD, PhD* Purpose Quantitative evaluation of passive tension of the intrinsic muscles of the hand is necessary to assess contracture of the intrinsic muscles accurately. The aim of this study was to evaluate the shear modulus, which is related to passive muscle tension, of the first dorsal interosseous (FDI) and first lumbrical (FL) muscles using shear wave elastography. Methods Subjects were 18 healthy males. The shear modulus of the FDI and FL muscles was assessed at several proximal interphalangeal (PIP), distal interphalangeal (DIP), metacarpophalangeal (MCP), and wrist joint positions. The position in which the MCP joint was flexed 60 past 0 with PIP-DIP joint extension and that in which the MCP joint was extended 30 past 0 with PIP-DIP joint flexion were respectively defined as the slack and stretched positions. We analyzed whether the shear modulus was affected by finger position (slack or stretched), wrist position (30 flexion past 0 and 30 extension past 0 ), and muscle (FDI or FL). Results Shear modulus in the stretched position was significantly higher than that in the slack position. The shear modulus of the FL muscle at 30 wrist extension was significantly higher than that at 30 flexion. The shear modulus of the FL muscle was significantly higher than that of the FDI muscle in the stretched position with the wrist at 30 flexion and extension, and in the slack position with the wrist at 30 extension. Conclusions The shear modulus of the FDI and FL muscles increased with MCP joint extension and PIP-DIP joint flexion. The difference in the muscle characteristics between the FDI and FL muscles should be considered when evaluating or treating contractures of the intrinsic muscles. Clinical relevance Shear wave elastography can evaluate the condition of the intrinsic muscles of the hand quantitatively. (J Hand Surg Am. 2019;-(-):1.e1-e8. Copyright Ó 2019 by the American Society for Surgery of the Hand. All rights reserved.) Key words hand intrinsic muscles, passive muscle tension, shear wave elastography.
T
HE INTRINSIC MUSCLES OF THE hand have an essential role in hand dexterity. The interosseous and lumbrical muscles originate from the metacarpals and flexor digitorum profundus
(FDP) tendons, respectively, and the tendons of these muscles comprise the lateral band, which inserts dorsally to the extensor apparatus. The intrinsic muscles function in metacarpophalangeal (MCP)
From the *Department of Orthopaedic Surgery and †Department of Public Health, Sapporo Medical University School of Medicine; the ‡Division of Rehabilitation, Sapporo Medical University Hospital; and the §Second Division of Physical Therapy, Sapporo Medical University School of Health Sciences, Sapporo; and the kDepartment of Physical Therapy, School of Rehabilitation Sciences, Health Science University of Hokkaido, Ishikari, Hokkaido, Japan.
No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.
Received for publication April 8, 2018; accepted in revised form January 14, 2019.
0363-5023/19/---0001$36.00/0 https://doi.org/10.1016/j.jhsa.2019.01.016
Corresponding author: Yudai Watanabe, PhD, Department of Orthopaedic Surgery, Sapporo Medical University School of Medicine, South 1, West 16, Chuo-ku, Sapporo, Hokkaido 060-8543, Japan; e-mail: [email protected].
Ó 2019 ASSH
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joint flexion and proximal interphalangeal (PIP)e distal interphalangeal (DIP) joint extension, and also contribute to grip and pinch strength.1 Several studies have indicated that strengthening and stretching of the intrinsic muscles may lead to improved hand dexterity, better fatigue endurance, and improved range of motion (ROM).2e4 Contracture of the intrinsic muscles causes severe impairment of hand function by generating an intrinsic-plus hand and swan neck deformities.5e7 Even in cases of mild contracture, patients may report tightness on PIP-DIP joint flexion with MCP joint extension and impaired hand dexterity.7 This contracture has been qualitatively evaluated by the intrinsic tightness test. In this test, when flexion of the PIP joint is limited with MCP joint extension, intrinsic tightness is present.5e9 Contracture of the intrinsic muscles has been treated by stretching exercises that emphasize MCP joint extension with PIPDIP joint flexion.8,9 However, qualitative methods are insufficient to evaluate the severity of contracture or the therapeutic effect of stretching exercises. Therefore, a quantitative evaluation method is needed that measures the passive muscle tension of the intrinsic muscles. Passive muscle stiffness has been estimated by the slope of forceemuscle length curve, based on the relation of joint angle and passive joint torque or displacement of the myotendinous junction using ultrasonography.10e12 However, these methods indirectly calculate the tension as a relative value. Recently, shear wave elastography has been used to assess the stiffness of soft tissue as the shear modulus without measuring the slope of the stressestrain curve. This apparatus uses transient and remote mechanical vibration generated by an acoustic radiation force at a localized area. The force causes tissue dislocation and generates a shear wave. Then, the apparatus calculates the shear modulus from the propagation of shear wave speed.13 In terms of muscle tissue, Maïsetti et al14 reported that the relation between the shear modulus and muscle length was highly correlated with the forceemuscle length curve. Moreover, Koo et al15 reported that the shear modulus was related to muscle force during passive stretching ex vivo. These studies indicated that passive muscle tension could be measured directly as an absolute value by shear wave elastography.16e22 We sought to evaluate the passive tension of the intrinsic muscles using this method, and to confirm tension with the muscle in a slack and stretched position. The specific aims of this study were to assess shear modulus in first dorsal interosseous (FDI) and first J Hand Surg Am.
lumbrical (FL) muscles in several MCP and PIP-DIP joint positions. In addition, we examined whether wrist position affected the shear modulus of the intrinsic muscles, because the lumbrical muscles originate from the FDP tendon, which changes tension according to wrist position. MATERIALS AND METHODS Subjects Subjects consisted of 18 healthy male volunteers (aged 30.9 4.3 years; range, 25e40 years). We excluded subjects from this study owing to (1) any abnormality of the right upper limb resulting from trauma, degenerative disease, or disorders of the central or peripheral nervous systems; and (2) hypermobility of the MCP joint of the index finger for which passive extension was more than 90 . The purpose and procedures of the study were explained to all subjects before participation. This study was approved by the ethics board of Sapporo Medical University. Protocols Subjects were placed in a sitting position with the shoulder at 0 adduction and the elbow at 90 flexion. To assess the shear modulus of the FDI and FL muscles, the forearm was pronated and supinated, respectively. The forearm was placed on a custom-made jig that could adjust the angle of the wrist joint and the MCP joint of the index finger. The forearm and fingers were immobilized with an orthosis and hook-and-loop fasteners. The PIP-DIP joint was set in 2 positions (full flexion and full extension) and the MCP joint in 4 positions (60 , 30 and 0 flexion past neutral, and 30 extension past 0 ). Shear modulus with the MCP joint at 60 flexion with PIP-DIP joint flexion could not be measured owing to the lack of space to position the probe. The position in which the MCP joint was at 60 flexion with PIP-DIP joint extension was defined as the slack position (Figs. 1A, 2A), and that in which the MCP joint was at 30 extension with PIP-DIP joint flexion was defined as the stretched position (Figs. 1G, 2G). There were 7 combinations of finger position (Figs. 1, 2) and the wrist position was set in 3 positions (30 flexion past 0 , neutral, and 30 extension past 0 ). In total, shear modulus was measured for 42 combinations (7 finger positions 3 wrist positions 2 muscles). The measurement order for the 6 positions (3 wrist positions 2 muscles) and 7 finger positions was randomized in advance. r
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FIGURE 1: Finger position for measurement of shear modulus of FDI muscle. A Metacarpophalangeal joint at 60 flexion with PIP-DIP joint extension. B Metacarpophalangeal joint at 30 flexion with PIP-DIP joint extension. C Metacarpophalangeal joint at 0 flexion with PIP-DIP joint extension. D Metacarpophalangeal joint at 30 extension with PIP-DIP joint extension. E Metacarpophalangeal joint at 30 flexion with PIP-DIP joint flexion. F Metacarpophalangeal joint at 0 flexion with PIP-DIP joint flexion. G Metacarpophalangeal joint at 30 extension with PIP-DIP joint flexion. (A) and (G) were defined as slack and stretched positions, respectively.
Shear modulus Shear modulus was measured by ultrasound shear wave elastography (version 4, AixPlorer, SuperSonic Imagine, Aix-en-Provence, France) with a linear array probe (50 mm, 4e15 MHz). The probe was applied to the dorsal and palmar hand to image the FDI and FL muscles, respectively, with acoustic gel (Fig. 3). The examiner manually operated the probe to maintain the shape of FDI and FL muscles. In anisotropic tissue such as muscle tissue, measurement of shear modulus changes by the position of the probe relative to the direction of the muscle fiber; it is recommended that it be measured in a longitudinal direction.23,24 The probe was set longitudinally along the direction of the muscle to observe the area of maximum muscle thickness. We analyzed ultrasonographic images of the FDI and FL muscles in accordance with the method reported by Infantolino et al25 and Jacobson26 (Fig. 4). The ultrasound device generated shear waves via the probe into the soft tissue and detected the shear wave propagation speed (c, m/s). Young’s modulus (E) was then calculated by the device as:
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E ¼ 3pc2
where p is the tissue density, which was assumed to be a constant 1,000 kg/m3 for human soft tissue.27 Young’s modulus was quantified based on an assumption of isotropic tissue; however, skeletal muscle cannot be assumed to be isotropic. In anisotropic tissue, measurement using the shear modulus rather than Young’s modulus is recommended.28 The shear modulus (G) was calculated as: G ¼ E = 2ð1 þ vÞ
where v is Poisson’s ratio, which is close to 0.5 for tissue assumed to be incompressible, such as skeletal muscle.19 Hence, we adopted the shear modulus as the value obtained by dividing Young’s modulus by 3. Young’s modulus was presented as a color-coded 15 15-mm2 region of interest (ROI) over a Bmode image. Within the ROI, a circular area was selected and the average Young’s modulus (in
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FIGURE 2: Finger positions for measurement of shear modulus of FL muscle. A Metacarpophalangeal joint at 60 flexion with PIP-DIP joint extension. B Metacarpophalangeal joint at 30 flexion with PIP-DIP joint extension. C Metacarpophalangeal joint at 0 flexion with PIP-DIP joint extension. D Metacarpophalangeal joint at 30 extension with PIP-DIP joint extension. E Metacarpophalangeal joint at 30 flexion with PIP-DIP joint flexion. F Metacarpophalangeal joint at 0 flexion with PIP-DIP joint flexion. G Metacarpophalangeal joint at 30 extension with PIP-DIP joint flexion. (A) and (G) were defined as slack and stretched positions, respectively.
kilopascals) was calculated for this area. The diameter of the circular area was set from 2 to 5 mm, depending on muscle thickness; the number of circles was set from 3 to 6 according to the ROI. The measurement value was derived from the average of the number of circular areas. We used the mean value of 2 measurements for statistical analysis.
positions. The root mean square of the EMG (RMSEMG) data was calculated for 100 milliseconds. The RMS-EMG was then calculated as the percentage of MVC (%MVC). The %MVC for the FL muscle was calculated using the same procedure. Range of motion Maximum passive ROM of the MCP joint with PIPDIP joint flexion or extension was measured after EMG was assessed.
Electromyography We confirmed that muscle activity had no effect on the measurement of the shear modulus using EMG. Surface EMG was measured after shear modulus measurement as follows: After the skin was cleaned with alcohol, the electrode (size: 1 6 mm; interelectrode distance: 12 mm; DL-141, S&ME, Tokyo, Japan) was placed in the same position as the probe. A reference electrode was placed over the styloid process of the ulna. The EMG data was simultaneously recorded using software (Labchart 7 Pro, AD Instruments, Sydney, Australia) via an analog-todigital converter (PowerLab 16/30, AD Instruments). After we measured the maximum voluntary contraction (MVC) of the FDI muscle, we recorded EMG data for the FDI muscle for 20 seconds in the 21 J Hand Surg Am.
Statistics For statistical analysis of the shear modulus data, we used 3-way analysis of variance with repeated measures for the finger position (slack and stretched), wrist position (30 flexion and 30 extension), and muscle (FDI and FL) with significance set at .05. A paired t test was performed for pairwise comparisons as a post hoc test. The Bonferroni correction with a significance level of .05 / 4 ¼ .0125 was applied. Measurement reliability between the first and second measurements for the 42 combinations was assessed using the intraclass correlation coefficient (ICC). r
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with the wrist at 30 flexion with the slack position was significantly higher than that with the wrist at 30 extension with the slack position (P ¼ .007). There was no significant difference between values obtained for the FDI muscle in the wrist at 30 flexion and extension with the stretched position (P ¼ .715). Shear modulus of the FL muscle was significantly higher than that of the FDI muscle with the wrist at 30 flexion (P ¼ .001) (Fig. 6B) and extension (P < .001) with the stretched position, and with the wrist at 30 extension with the slack position (P ¼ .001). There was no significant difference between values obtained for the FL and FDI muscles with the wrist at 30 flexion in the slack position (P ¼ .550). The ICC between the first and second measurements for the 42 combinations ranged from 0.808 to 0.988. In addition, all %MVC data were less than 3.2% and mean values for the FDI and FL muscles ranged from 0.71% to 1% and from 1.16% to 1.57%, respectively.
FIGURE 3: Measurement method for the shear modulus of FL and FDI muscles by ultrasound shear wave elastography. The forearm was placed on a custom-made jig that allowed adjustment of the angle of the wrist and MCP joint of the index finger. The forearm and fingers were immobilized with an orthosis and hook-and-loop fasteners. The linear array probe was applied to the dorsal and palmar hand to image the A FDI and B FL muscles, respectively, with acoustic gel.
DISCUSSION We evaluated passive tension of the FDI and FL muscles quantitatively by measuring the shear modulus value at various finger and wrist joint positions. In particular, we found that the shear modulus for the FDI and FL muscles increased with MCP joint extension and PIP-DIP joint flexion. This result indicated that the intrinsic tightness test and the manner in which this position is used for stretching exercises for the intrinsic muscles are valuable for assessing and treating intrinsic muscles contracture. The shear modulus of FL muscle was higher than that of the FDI muscle in the stretching position. This result suggests that the intrinsic tightness test is likely to reflect lumbrical muscle more than interosseous muscle tightness. In addition, contracture of the lumbrical muscle would be discriminated by the wrist position because the shear modulus of the FL muscle became higher with wrist extension. Therefore, we think that this quantitative evaluation would be useful for analyzing the intrinsic tightness test more accurately. Interestingly, the shear modulus of the FL muscle increased significantly with wrist and MCP joint extension. A possible explanation for this is that the shear modulus of the FL was affected by tension in the FDP tendon, which is the origin of the lumbrical muscles. Tension in the FDP tendon increases with MCP and wrist joint extension,29 and this might be transmitted to the shear modulus of the lumbrical muscle. In addition, the shear modulus of the FDI
RESULTS Three subjects were excluded from the original pool of 21 because stable color-coded maps for the FL muscle in 2 subjects and a clear B-mode image of the FL muscle in 1 could not be measured. We obtained complete data for 18 of the 21 subjects. Maximum passive flexion angle of the MCP joint with PIP-DIP joint flexion and extension was 89.7 8.3 and 93.1 8.9 , respectively. Maximum passive extension angle of the MCP joint with PIP-DIP joint flexion and extension was 56.4 8.4 and 60.6 7.6 , respectively. Minimum and maximum shear modulus values for the FDI and FL muscles were obtained in the slack and stretched positions, respectively, regardless of wrist position (Fig. 5). There were significant interactions in the shear modulus value among finger position, wrist position, and muscle (P < .001; 3-way analysis of variance). The shear modulus in the stretched position (MCP joint at 30 extension with PIP-DIP flexion) was significantly higher than that in the slack position (MCP joint at 60 flexion with PIP-DIP extension) independent of wrist position and muscle (P < .001). Shear modulus of the FL muscle in the wrist at 30 extension was significantly higher than that at 30 flexion with both the slack and stretched positions (P .001) (Fig. 6A). Shear modulus of the FDI muscle J Hand Surg Am.
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FIGURE 4: Ultrasonographic findings for FDI and FL muscles. A The FDI muscle was identified as the muscle tissue above the FDI tendon originating from the second metacarpal head. The color-coded region of interest (ROI) indicates the shear modulus. The average of Young’s modulus was calculated for circular area within the ROI. The ROI was set at areas with the maximum observable muscle thickness. B The FL muscle was identified at the same depth as the flexor tendon. The right end of the ROI was set in the same position as the right end of the adductor pollicis muscle.
FIGURE 5: Shear modulus of FDI and FL muscles at various finger and wrist positions. A Shear modulus of the FDI muscle. B Shear modulus of the FL muscle. The minimum shear modulus value was obtained with the MCP joint at 60 flexion with PIP-DIP joint extension in all wrist positions. The maximum shear modulus value was obtained with the MCP joint at 30 extension with PIP-DIP joint flexion in all wrist positions. PIPDIPExt, PIP-DIP joint extension; PIPDIPFlex, PIP-DIP joint flexion; WE, wrist at 30 extension; WF, wrist at 30 flexion; WN, wrist in neutral position.
muscle in the slack position slightly but significantly increased with wrist flexion. The interosseous muscles insert into the extensor digitorum communis tendon, and tension in that tendon, which is increased by MCP joint and wrist flexion, could be transmitted to the interosseous muscles. Thus, the shear modulus of the FDI and FL muscles is affected by wrist position. These results indicate that the wrist position should be taken into consideration when assessing contracture of the intrinsic muscles. Moreover, we recommend that wrist position be fixed when measuring the shear modulus of the FDI and FL muscles by shear wave elastography.
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Shear modulus of the FL muscle in the stretched position was higher than that of the FDI muscle. Koo and Hug30 suggested that the shear modulus was primarily affected by the muscle cross-sectional area, with which it was negatively correlated. Jacobson et al31 reported that the cross-sectional area of the FDI and FL muscles was 1.50 and 0.11 cm2, respectively, which corresponded to the results of their study. Hirata et al32 suggested that stretching notably affects muscles with the highest shear modulus value. Based on these and our studies, stretching exercises might have a more marked effect on the FL muscle than on the FDI muscle.
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FIGURE 6: Post hoc analysis after 3-way analysis of variance for the shear modulus values for the FDI and FL muscles. A Comparison of the shear modulus between 30 flexion and 30 extension of the wrist. B Comparison of the shear modulus between the FDI and FL muscles. FSL, finger slack position; FST, finger stretched position; WE, wrist at 30 extension; WF, wrist at 30 flexion. *P < .0125.
Recently, several studies20e22,32,33 indicated a decrease in the shear modulus after stretching exercises in healthy subjects, and those changes depended on the different rehabilitation programs. In treating intrinsic muscles contracture, it is important to compare clinical status before and after treatment. Further study is required to evaluate the therapeutic effect from the viewpoint of the shear modulus of intrinsic muscles. We separately assessed the shear modulus and EMG of the FDI and FL muscles, the size of which was too small to position the probe and the EMG recorder simultaneously. It is controversial whether the threshold of EMG activity (%MVC) of a muscle could affect the shear modulus. In this study, the change in %MVC of the FDI and FL muscles was only 0.29% and 0.41%, respectively, during passive joint movement. These results indicated that EMG activity has little effect on the shear modulus. We conclude that the current data are reliable and accurate. There were several limitations to this study. First, the shear modulus of the FL muscle could not be assessed in 3 subjects. This was probably because of the thickness of the skin or the existence of palmar fascia. Second, this study demonstrated the shear modulus of only the FDI and FL muscles. The other intrinsic muscles of the hand would not necessarily have had identical results. Third, we could not constantly set the probe in the same position. Miyamoto et al34 reported that the difference in the shear modulus value was negligible when the probe is positioned parallel to the fascicle and at 20 oblique to the fascicle, whereas Maïsetti et al14 indicated that an increase in probe rotation affected accurate measurement of the shear modulus. In the current study, the ICC between the first and second measurements J Hand Surg Am.
was greater than 0.8. We conclude that setting the probe by hand has little influence on measurements of the shear modulus. We measured the shear modulus of the FDI and FL muscles by shear wave elastography in various positions of the PIP-DIP, MCP, and wrist joints. The shear modulus of each muscle increased with MCP joint extension and PIP-DIP joint flexion. The shear modulus of each muscle was also affected by wrist position. We found that passive tension of the FL muscle was higher than that of the FDI muscle. The results of our study suggest that quantitative evaluation using shear wave elastography could allow more accurate evaluation of the severity of contracture and of the therapeutic effect of stretching. REFERENCES 1. Kozin SH, Porter S, Clark P, Thoder JJ. The contribution of the intrinsic muscles to grip and pinch strength. J Hand Surg Am. 1999;24(1):64e72. 2. Less M, Krewer SE, Eickelberg WW. Exercise effect on strength and range of motion of hand intrinsic muscles and joints. Arch Phys Med Rehabil. 1977;58(8):370e374. 3. Penn IW, Chuang TY, Chan RC, Hsu TC. EMG power spectrum analysis of first dorsal interosseous muscle in pianists. Med Sci Sports Exerc. 1999;31(12):1834e1838. 4. Olafsdottir HB, Zatsiorsky VM, Latash ML. The effects of strength training on finger strength and hand dexterity in healthy elderly individuals. J Appl Physiol (1985). 2008;105(4):1166e1178. 5. Finochietto R. Retracción de Volkmann de los músculos intrínsecos de la mano. Bol Trab Soc Cir B Aires. 1920;4:31e37. 6. Bunnell S, Doherty EW, Curtis RM. Ischemic contracture, local, in the hand. Plast Reconstr Surg (1946). 1948;3(4):424e433. 7. Tosti R, Thoder JJ, Ilyas AM. Intrinsic contracture of the hand: diagnosis and management. J Am Acad Orthop Surg. 2013;21(10): 581e591. 8. McEntee PM. Therapist’s management of the stiff hand. In: Hunter JM, Schneider LH, Mackin EJ, Callahan AD, eds. Rehabilitation of the Hand: Surgery and Therapy. 3rd ed. St. Louis, MO: Mosby; 1990:328e341. 9. Seu M, Pasqualetto M. Hand therapy for dysfunction of the intrinsic muscles. Hand Clin. 2012;28(1):87e100.
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22. Miyamoto N, Hirata K, Kanehisa H. Effects of hamstring stretching on passive muscle stiffness vary between hip flexion and knee extension maneuvers. Scand J Med Sci Sports. 2017;27(1):99e106. 23. Gennisson JL, Deffieux T, Macé E, Montaldo G, Fink M, Tanter M. Viscoelastic and anisotropic mechanical properties of in vivo muscle tissue assessed by supersonic shear imaging. Ultrasound Med Biol. 2010;36(5):789e801. 24. Alfuraih AM, O’Connor P, Tan AL, Hensor E, Emery P, Wakefield RJ. An investigation into the variability between different shear wave elastography systems in muscle. Med Ultrason. 2017;19(4):392e400. 25. Infantolino BW, Challis JH. Measuring subject specific muscle model parameters of the first dorsal interosseous in vivo. Ann Biomed Eng. 2014;42(6):1331e1339. 26. Jacobson JA. Fundamentals of Musculoskeletal Ultrasound. Philadelphia, PA: Saunders; 2007. 27. Gennisson JL, Cornu C, Catheline S, Fink M, Portero P. Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech. 2005;38(7):1543e1550. 28. Royer D, Gennisson JL, Deffieux T, Tanter M. On the elasticity of transverse isotropic soft tissues (L). J Acoust Soc Am. 2011;129(5): 2757e2760. 29. Tanaka T, Amadio PC, Zhao C, Zobitz ME, An KN. Flexor digitorum profundus tendon tension during finger manipulation. J Hand Ther. 2005;18(3):330e338. 30. Koo TK, Hug F. Factors that influence muscle shear modulus during passive stretch. J Biomech. 2015;48(12):3539e3542. 31. Jacobson MD, Raab R, Fazeli BM, et al. Architectural design of the human intrinsic hand muscles. J Hand Surg Am. 1992;17(5):804e809. 32. Hirata K, Miyamoto-Mikami E, Kanehisa H, Miyamoto N. Musclespecific acute changes in passive stiffness of human triceps surae after stretching. Eur J Appl Physiol. 2016;116(5):911e918. 33. Yamauchi T, Hasegawa S, Nakamura M, et al. Effects of two stretching methods on shoulder range of motion and muscle stiffness in baseball players with posterior shoulder tightness: a randomized controlled trial. J Shoulder Elbow Surg. 2016;25(9):1395e1403. 34. Miyamoto N, Hirata K, Kanehisa H, Yoshitake Y. Validity of measurement of shear modulus by ultrasound shear wave elastography in human pennate muscle. PLoS One. 2015;10:e0124311.
10. Toft E, Espersen GT, Kålund S, Sinkjaer T, Hornemann BC. Passive tension of the ankle before and after stretching. Am J Sports Med. 1989;17(4):489e494. 11. Morse CI, Degens H, Seynnes OR, Maganaris CN, Jones DA. The acute effect of stretching on the passive stiffness of the human gastrocnemius muscle tendon unit. J Physiol. 2008;586(1):97e106. 12. Hwang W, Kelly NG, Boriek AM. Passive mechanics of muscle tendinous junction of canine diaphragm. J Appl Physiol (1985). 2005;98(4):1328e1333. 13. Nowicki A, Dobruch-Sobczak K. Introduction to ultrasound elastography. J Ultrason. 2016;16(65):113e124. 14. 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(6): 978e984. 15. Koo TK, Guo JY, Cohen JH, Parker KJ. Relationship between shear elastic modulus and passive muscle force: an ex-vivo study. J Biomech. 2013;46(12):2053e2059. 16. Hirata K, Kanehisa H, Miyamoto-Mikami E, Miyamoto N. Evidence for intermuscle difference in slack angle in human triceps surae. J Biomech. 2015;48(6):1210e1213. 17. Lacourpaille L, Hug F, Nordez A. Influence of passive muscle tension on electromechanical delay in humans. PLoS One. 2013;8: e53159. 18. Koo TK, Guo JY, Cohen JH, Parker KJ. Quantifying the passive stretching response of human tibialis anterior muscle using shear wave elastography. Clin Biomech (Bristol, Avon). 2014;29(1):33e39. 19. Eby SF, Cloud BA, Brandenburg JE, et al. Shear wave elastography of passive skeletal muscle stiffness: influences of sex and age throughout adulthood. Clin Biomech (Bristol, Avon). 2015;30(1): 22e27. 20. Taniguchi K, Shinohara M, Nozaki S, Katayose M. Acute decrease in the stiffness of resting muscle belly due to static stretching. Scand J Med Sci Sports. 2015;25(1):32e40. 21. Andrade RJ, Lacourpaille L, Freitas SR, McNair PJ, Nordez A. Effects of hip and head position on ankle range of motion, ankle passive torque, and passive gastrocnemius tension. Scand J Med Sci Sports. 2016;26(1):41e47.
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