- Email: [email protected]
Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging
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MODEL
Journal of Bodywork & Movement Therapies (2016) xx, 1e5
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.elsevier.com/jbmt
HUMAN PHYSIOLOGY STUDY
Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging Shintarou Kudo, RPT, PhD a,*, Sho Nakamura, RPT b a b
Department of Physical Therapy, Morinomiya University of Medical Sciences, Japan Department of Rehabilitation, Miyamoto Orthopedics Clinic, Japan
Received 22 June 2016; received in revised form 4 August 2016; accepted 10 August 2016
KEYWORDS Ultrasound imaging; Vastus lateralis; Hardness
Summary The aims of this study were to clarify the relationship between deformation of the VL during knee flexion and the stiffness of the VL. 40 lower limbs of 20 male normal volunteers were divided into control and tightness groups using the Ely test. Deformation of the VL in the transverse plane during active knee flexion from 0 to 90 was recorded using B-mode ultrasonography. Hardness of the VL was measured on the middle lateral thigh using a durometer. The reaction force at fully passive flexion was measured using a hand held dynamometer. The deformation of the VL and the hardness and passive torque showed significant differences between the 2 groups. The deformation of the VL showed a significantly higher correlation with hardness of the VL. Measurements of the deformation of the VL might be predicted by the elasticity around the VL. ª 2016 Elsevier Ltd. All rights reserved.
Introduction Many physical therapists, athletic trainers, and biomechanists are interested in the morphological changes that occur in skeletal muscles during physical activity. Morphological changes are difficult to quantitate, therefore, physical therapists have used manual therapy * Corresponding author. Department of physical therapy, Morinomiya University of Medical Sciences, Nankokita1-26-16, Suminoe Ward, Osaka City, Osaka, Japan. E-mail address: [email protected] (S. Kudo).
combined with imaging to monitor those changes. Ultrasonography (US) has been incorporated in the rehabilitation of muscle-skeletal disorders, such as rotator cuff tears, biceps brachialis long head tendinitis, and low back pain (Bailey et al., 2015; Hellem et al., 2015; Kiesel et al., 2007; Teyhen et al., 2007). And has been recognized as a very useful method to assess skeletal muscle under both the static and dynamic conditions (Whittaker and Emery, 2014; Koppenhaver et al., 2009). Neuromuscular deficits have been linked with chronic musculoskeletal conditions. Rehabilitative ultrasound imaging (RUSI) has been used to assist in the rehabilitation
http://dx.doi.org/10.1016/j.jbmt.2016.08.006 1360-8592/ª 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
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MODEL
2 of neuro-musculoskeletal disorders and to evaluate morphology and function of the skeletal muscle and soft tissue during exercise and physical tasks. RUSI is used to assist in the application of therapeutic interventions, and provides feedback to patients and physical therapists (Teyhen, 2006). However, US of skeletal muscle in many clinical settings has been under static conditions. US can capture dynamic images of soft tissue during movement and motion, but there are challenges including difficulty in fixing the transducer to body segments, interpretation of the deformation of the skeletal muscle mean, and the establishment of standard values of the deformation of the skeletal muscle under regular dynamic conditions. The dynamics of the gastrocnemius muscle exhibit isometric contractions during motions such as walking, jumping, and running when assessed using US with a transducer fixed to the subject’s leg (Fukunaga et al., 2001; Kawakami et al., 2002). Previously, we demonstrated that the dynamics of the medial head of the gastrocnemius muscle show inhibited isometric contraction during the dorsiflexion phase of the eccentric calf raise exercise using a fixed transducer on the leg (Kudo et al., 2015). In addition, skeletal muscle contraction has a role in the power generation of the motion, stabilizing the joints during joint movements, and maintaining body temperature. Through concentric contraction, the muscle is shortened in the longitudinal direction and expanded in the transverse direction. Skeletal muscles are comprised of muscle fascicles, tendons, vessels, and myofascia. The myofascia forms a network throughout the body that covers and links all organs, muscles, and nerves. It also acts as a buffer when muscle and myofibrils glide and functions as a support for traversing blood vessels, nerves, and lymphatic vessels (Schleips et al., 2012). Loose connective tissue rich in hyaluronic acid and with varying fiber directions acts as a buffer that enables the tissue to glide (Stecco et al., 2011). We hypothesized that when the elasticity of loose connective tissue of the myofascia has been changed pathologically, there is an associated decrease in the deformation of the skeletal muscle during joint motion and an increase in muscle hardness. However, no consensus standardized values of skeletal muscle deformation during joint motion have been established. Thus, skeletal deformation cannot be assessed effectively using US in the clinical setting. The vastus lateralis muscle (VL) originates at the lateral lip of the linea aspera of the femur and inserts at the tibial tubercle. The VL acts a strong extensor of the knee, and an increase in the hardness of the VL can lead to anterior knee pain syndrome such as patelofemoral joint arthritis and jumper’s knee. Therefore, evaluation of the hardness of the VL is important. However, this evaluation depends on palpation of the VL, which is not an objective method. No quantitative methods have been identified to evaluate the hardness of the VL. The aims of this study were to clarify the relationship between deformation of the VL during knee flexion and the hardness of the VL. Moreover the cut off value, which can assess decreased deformation of the VL, was estimated.
S. Kudo, S. Nakamura
Methods Forty lower limbs of 20 male normal volunteers participated in this study. All of the volunteers provided informed consent. The volunteers were divided into control and tightness groups using the Ely test. Twenty limbs of 10 subjects who showed a negative score on the Ely test were assigned to the control group, and the other 20 limbs of 10 subjects who showed a positive score on the Ely test were assigned to the tightness group. The Ely test was performed one time by a physical therapist who had 8years clinical experiences in orthopedics physical therapy. Positive Ely test was defined as the condition which could not be touched the own heel to the buttocks with keeping the bilateral anterior superior iliac spina contact to the bed in prone lying. General characteristics of all subjects are shown in Table 1. This study was approved by the ethics committee of our university. Deformation of the VL in the transverse plane during active knee flexion from 0 to 90 was recorded using Bmode US (Mylab25; Esaote, Indianapolis, IN, USA) with a 12 MHz liner probe fixed on the lateral side of the distal one third of the thigh by an original fixation device. Movement of the postero-lateral corner of the VL in the US image from 0 to 90 degrees of knee flexion was measured using Image-J (NIH) (Fig. 1). Deformation of the VL was measured 3 times, and the mean value was accepted. Hardness of the VL was measured using a durometer (TDM-NA1(DX) TRY-ALL INC., Japan) and a hand held dynamometer (mtus F-1, Anima co., Japan). For the durometer measurement, a single examiner performed 3 repetitions to measure the hardness on the middle lateral thigh in the supine position with the knee extended. In the torque meter measurement, the subject’s knee was fully flexed and held by a single examiner using a jig with a hand held dynamometer. Subjects were positioned as prone and relaxed and their pelvis and thigh were fixed on a bed using a hard polyester band. The axis of the jig was set on the knee joint axis, and the hand held dynamometer was set on the distal end of the leg. The reaction force at fully passive flexion, assessed by a single examiner, divided by the leg length was calculated, and the mean value of the reaction force over 5 repetitions was determined as the passive torque. The muscle tenderness at the lateral side of the middle thigh was evaluated by a single examiner using an algometer (FP meter, Matsumiya co., Japan). All parameters were measured in 3 repetitions, and the average of the 3 measurement values was accepted. All measurements were repeated 3 times to assess test-retest reliability (10
Table 1
General characteristic data.
Age (y/o) Height (cm) Weight (kg) BMI
All
Control group
Tightness group
P-value
20.0 2.3 167.4 5.8 59.9 6.9 20.4 2.4
19.1 0.9 170.4 6.4 57.2 7.3 19.6 2.3
20.1 2.4 167.4 6.1 59.9 7.3 21.4 2.3
0.23 0.22 0.42 0.1
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
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Relationship between hardness and deformation of the vastus lateralis
3
Figure 1 US image of the VL deformation. Postero-lateral corner of the VL was moved to postero-lateral direction during active knee flexion. (a; US image of the VL at 0 degree of knee. b; US image of the VL at 90 flexion of knee. VL; Vastus Lateralis. BF; Biceps Femoris. F: Femur. l; distance postero-lateral corner of the VL from 0 to 90 degree of the knee.)
healthy males; mean age, 21.2 2.1 y/o; mean height, 168.5 4.8 cm; mean weight, 58.4 6.9 kg). The muscle hardness, tenderness, passive torque, and deformation of the VL were compared between the 2 groups using the ManneWhitney test. The relationship between the deformation of the VL and the other 3 parameters were investigated using the Spearman correlation coefficient. Moreover, both the sensitivity and specificity of the morphological changes of the VL were calculated, and the ROC curve was drawn. Cut-off values were determined by the Yonden index. The reliability of the dynamics of the VL was examined using intraclass correlation coefficients (ICC), and the standard error of measurement (SEM) was calculated. All statistical methods were performed using R2.8.1 (free software).
of control group. However, the tenderness of the VL was not significantly different between the 2 groups. The correlation values between the deformation of the VL and the other parameters are shown in Table 3. The deformation of the VL showed a significantly higher correlation with hardness of the VL using the durometer, with significant mild correlation with passive torque in terminal knee flexion. However, there was no significant correlation between deformation of the VL and tenderness. The area of under the curve of the ROC curve concerning deformation of the VL was 0.9, and the cut-off value was 12.5 mm based on the Youden index. Both sensitivity and specificity of the cut off value were 0.95, respectively.
Discussion Results The ICC of the deformation of the VL was 0.92, and the SEM was 0.41 mm. The mean values of the passive torque, the deformation of the VL, the tenderness, and the hardness of both groups were shown in Table 2. The deformation of the VL of the tightness group was significantly decreased with that of control group. And hardness of the VL and passive torque of the tightness were significant smaller than those
Table 2 Difference of the parameter between control and tightness group.
Passive torque (N) Deformation of the VL (mm) Tenderness (kg) Hardness (N)
Control group
Tightness group
P-value
124.1 19.3 1.5 0.2
249.8 24.9 0.9 0.2
<0.001 <0.001
A high viscoelasticity of the skin, fascia, subcutaneous tissue (adipose tissue, dense and loose connective tissue), myofascia, and muscle is required during joint motion. The subcutaneous tissues help buffer the friction force (Stecco, 2015). Moreover, the intermuscular connective tissue mediates significant interactions between adjacent muscles (Huijing and Baan, 2001). The force between adjacent muscles may be influenced by the deformation of the muscle during motion through inter-muscular connective tissue. In the clinical setting, therapists perform muscle stretching for patients with restricted range of joint motion, in order to increase the elasticity of the skeletal
Table 3 Correlation of the deformation and the other parameter.
Deformation of the VL 4.4 0.5 34.6 1.8
4.5 0.9 42.3 3.2
0.61 <0.001
- Passive torque - Hardness - Tenderness
r
P-value
0.51 0.74 0.01
<0.001 <0.001 0.92
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
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4 muscle. However, the elasticity of skeletal muscle is due not only to muscle fascicles, but also to connective tissue around the skeletal muscle such as myofascia. The hardness of skeletal muscles is affected by surrounding structures. Therefore, it is important to assess the hardness of the connective tissue around the muscle. Recent studies highlight the connections of muscle with the dense connective tissue of the locomotor system, commonly referred to as fascia (Stecco et al., 2009; Huijing, 2009). Muscles can stretch the fascia in a longitudinal sense through expansions that stem from the tendons. They can also stretch fascia in a transversal sense through the intramuscular connective tissue (endomysium, perimysium, and epimysium) (Huijing and Jaspers, 2005; Purslow, 2010) and through the dense connective tissue of the musculoskeletal system (intermuscular septum, neurovascular bundles). However, the elasticity of those connective tissues cannot be measured using previously available methods. In this study, the tightness group identified using the Ely test showed significantly decreased muscle deformation of the VL and increased passive torque and hardness compared to that of the control group. Tenderness of pain was not significantly different between the 2 groups. These results suggest that the deformation of the VL observed during knee flexion using US correlates with the hardness of the VL. Moreover, the deformation of the VL showed a strong correlation with hardness assessed using a durometer, and showed a mild correlation with passive torque. The durometer measured muscle hardness through the skin and subcutaneous tissue. Therefore, the values obtained may not reflect only the hardness of the muscle (Ichilkawa et al., 2015), but also the hardness the skin and subcutaneous tissue. The passive torque of the muscle reflects predominately the elasticity of the muscle. Therefore, the deformation of the VL using US indicates the hardness of both the muscle and subcutaneous tissue around the muscle. Measurements of the deformation of the VL may be predicted by the elasticity around the VL. Increased hardness of the VL can lead to anterior knee pain syndrome. The Ely test in the clinical setting should be performed when the hardness of the VL is suspected. However, if patients have other impairments of the knee, such as osteoarthritis, the Ely test cannot be performed because the range of flexion of the knee is restricted. In these cases, dynamics of the VL are able to assess the flexibility of the VL quantitatively. The cut off value of the deformation of the VL was 12.5 mm. It can assess increasing hardness of the VL, when deformation of the VL was less than 12.5 mm. This study have two limitations. One is analysis of this study is a two dimensional analyses of muscle deformation, although the dynamics of the VL are shown as three dimensional movement in vivo. Therefore, deformation of the VL in this study was not defined by movements of identical points from 0 to 90 degrees of knee flexion, but was estimated from longitudinal changes during VL movement. Another is the Ely test is performed one time only. Ely test has a sensitivity ranging from 56 to 59% and the specificity ranging from 64 to 85% when assess the spasticity of the quadriceps in the cerebral palsy (Marks et al., 2003). However the Ely test is widely used methods which has high
S. Kudo, S. Nakamura reliability (Piva et al., 2006) for assessing the tightness of the quadriceps in the clinical setting. Therefore, decreasing deformation of the VL can be assessed the decreasing elasticity around the VL, although a processing that subjects are divided into two groups have a bias in this study.
References Bailey, L.B., Beattie, P.F., Shanley, E., Seitz, A.L., Thigpen, C.A., 2015. Current rehabilitation applications for shoulder ultrasound imaging. J. Orthop. Sports Phys. Ther. 45 (5), 394e405. Fukunaga, T., Kubo, K., Kawakami, Y., Fukashiro, S., Kanehisa, H., Maganaris, C.N., 2001. In vivo behavior of human muscle tendon during walking. Proc. Biol. Soc. 268 (1464), 229e233. Hellem, A.R., Hollman, J.H., Sellon, J.L., Pourcho, A., Strauss, J., Smith, J., 2015. Ultrasound evaluation of the lower trapezius in adolescent baseball pitchers. PM R. 15, 01032-1. Huijing, P.A., Baan, G.C., 2001. Myofascial force transmission causes interaction between adjacent muscles and connective tissue: effects of blunt dissection and compartmental fasciotomy on length force characteristics of rat extensor digitorum longus muscle. Arch. Physiol. Biochem. 109 (2), 97e109. Huijing, P.A., Jaspers, R.T., 2005. Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand. J. Med. Sci. Sports 15 (6), 349e380. Huijing, P.A., 2009. Epimuscular myofascial force transmission: a historical review and implications for new research. J. Biomech. 42 (1), 9e21. Ichilkawa, K., Takei, H., Usa, H., Mitomo, S., Ogawa, D., 2015. Comparative analysis of ultrasound changes in the vastus lateralis muscle following myofascial release and thermotherapy: a pilot study. J. Bodyw. Mov. Ther. 19 (2), 327e336. Kawakami, Y., Muraoka, T., Ito, S., Kanehisa, H., Fukunaga, T., 2002. In vivo muscle fiber behavior during counter movement exercise in humans reveals a significant role for tendon elasticity. J. Physiol. 540, 635e646. Kiesel, K.B., Uhl, T.L., Underwood, F.B., Rodd, D.W., Nitz, A.J., 2007. Measurement of lumbar multifidus muscle contraction with rehabilitative ultrasound imaging. Man. Ther. 12 (2), 161e166. Koppenhaver, S.L., Hebert, J.J., Parent, E.C., Fritz, J.M., 2009. Rehabilitative ultrasound imaging is a valid measure of trunk muscle size and activation during most isometric sub-maximal contractions: a systematic review. Aust. J. Physiother. 55 (3), 153e169. Kudo, S., Hisada, T., Sato, T., 2015. Determination of the fascicle length of the gastrocnemius muscle during calf raise exercise using ultrasonography. J. Phys. Ther. Sci. 12, 3763e3766. http: //dx.doi.org/10.1589/jpts.27.3763. Marks, M.C., Alexander, J., Sutherland, D.H., Chambers, H.G., 2003. Clinical utility of the Duncan-Ely test for rectus femoris dysfunction during the swing phase of gait. Dev. Med. Child. Neurol. 45 (11), 763e768. Piva, S.R., Fitzgerald, K., Irrgang, J.J., Jones, S., Hando, B.R., Browder, D.A., Childs, J.D., 2006. Reliability of measures of impairments associated with patellofemoral pain syndrome. BMC Musculoskelet. Disord. 31 (7), 33. http: //dx.doi.org/10.1186/1471-2474-7-33. Purslow, P.P., 2010. Muscle fascia and force transmission. J. Bodyw. Mov. Ther. 14 (4), 411e417. Schleips, R., Findley, T.W., Chaitow, L., Huijing, P., 2012. Fascia: the Tensional Network of the Human Body, first ed. Churchill Livingstone, London,UK. Stecco, A., Macchi, V., Stecco, C., Porzionato, A., Ann Day, J., Delmas, V., De Caro, R., 2009. Anatomical study of myofascial
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
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Relationship between hardness and deformation of the vastus lateralis continuity in the anterior region of the upper limb. J. Bodyw. Mov. Ther. 13 (1), 53e62. Stecco, C., Stern, R., Porzionato, A., Macchi, V., Masiero, S., Stecco, A., De Caro, R., 2011. Hyaluronan within fascia in the etiology of myofascial pain. Surg. Radiol. Anat. 33 (10), 891e896. Stecco, C., 2015. Functional Atlas of the Human Fascial System, first ed. Churchil livingstone, London,UK. Teyhen, D.S., 2006. Rehabilitative ultrasound imaging symposium. J. Orthop. Sports Phys. Ther. 36 (8), A1eA3.
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Teyhen, D.S., Gill, N.W., Whittaker, J.L., Henry, S.M., Hides, J.A., Hodges, P., 2007. Rehabilitative ultrasound imaging of the abdominal muscles. J. Orthop. Sports Phys. Ther. 37 (8), 450e466. Whittaker, J.L., Emery, C.A., 2014. Sonographic measures of the gluteus medius, gluteus minimus, and vastus medialis muscles. J. Orthop. Sports Phys. Ther. 44 (8), 627e632. http: //dx.doi.org/10.2519/jospt.2014.5315.
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
MODEL
Journal of Bodywork & Movement Therapies (2016) xx, 1e5
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.elsevier.com/jbmt
HUMAN PHYSIOLOGY STUDY
Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging Shintarou Kudo, RPT, PhD a,*, Sho Nakamura, RPT b a b
Department of Physical Therapy, Morinomiya University of Medical Sciences, Japan Department of Rehabilitation, Miyamoto Orthopedics Clinic, Japan
Received 22 June 2016; received in revised form 4 August 2016; accepted 10 August 2016
KEYWORDS Ultrasound imaging; Vastus lateralis; Hardness
Summary The aims of this study were to clarify the relationship between deformation of the VL during knee flexion and the stiffness of the VL. 40 lower limbs of 20 male normal volunteers were divided into control and tightness groups using the Ely test. Deformation of the VL in the transverse plane during active knee flexion from 0 to 90 was recorded using B-mode ultrasonography. Hardness of the VL was measured on the middle lateral thigh using a durometer. The reaction force at fully passive flexion was measured using a hand held dynamometer. The deformation of the VL and the hardness and passive torque showed significant differences between the 2 groups. The deformation of the VL showed a significantly higher correlation with hardness of the VL. Measurements of the deformation of the VL might be predicted by the elasticity around the VL. ª 2016 Elsevier Ltd. All rights reserved.
Introduction Many physical therapists, athletic trainers, and biomechanists are interested in the morphological changes that occur in skeletal muscles during physical activity. Morphological changes are difficult to quantitate, therefore, physical therapists have used manual therapy * Corresponding author. Department of physical therapy, Morinomiya University of Medical Sciences, Nankokita1-26-16, Suminoe Ward, Osaka City, Osaka, Japan. E-mail address: [email protected] (S. Kudo).
combined with imaging to monitor those changes. Ultrasonography (US) has been incorporated in the rehabilitation of muscle-skeletal disorders, such as rotator cuff tears, biceps brachialis long head tendinitis, and low back pain (Bailey et al., 2015; Hellem et al., 2015; Kiesel et al., 2007; Teyhen et al., 2007). And has been recognized as a very useful method to assess skeletal muscle under both the static and dynamic conditions (Whittaker and Emery, 2014; Koppenhaver et al., 2009). Neuromuscular deficits have been linked with chronic musculoskeletal conditions. Rehabilitative ultrasound imaging (RUSI) has been used to assist in the rehabilitation
http://dx.doi.org/10.1016/j.jbmt.2016.08.006 1360-8592/ª 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
+
MODEL
2 of neuro-musculoskeletal disorders and to evaluate morphology and function of the skeletal muscle and soft tissue during exercise and physical tasks. RUSI is used to assist in the application of therapeutic interventions, and provides feedback to patients and physical therapists (Teyhen, 2006). However, US of skeletal muscle in many clinical settings has been under static conditions. US can capture dynamic images of soft tissue during movement and motion, but there are challenges including difficulty in fixing the transducer to body segments, interpretation of the deformation of the skeletal muscle mean, and the establishment of standard values of the deformation of the skeletal muscle under regular dynamic conditions. The dynamics of the gastrocnemius muscle exhibit isometric contractions during motions such as walking, jumping, and running when assessed using US with a transducer fixed to the subject’s leg (Fukunaga et al., 2001; Kawakami et al., 2002). Previously, we demonstrated that the dynamics of the medial head of the gastrocnemius muscle show inhibited isometric contraction during the dorsiflexion phase of the eccentric calf raise exercise using a fixed transducer on the leg (Kudo et al., 2015). In addition, skeletal muscle contraction has a role in the power generation of the motion, stabilizing the joints during joint movements, and maintaining body temperature. Through concentric contraction, the muscle is shortened in the longitudinal direction and expanded in the transverse direction. Skeletal muscles are comprised of muscle fascicles, tendons, vessels, and myofascia. The myofascia forms a network throughout the body that covers and links all organs, muscles, and nerves. It also acts as a buffer when muscle and myofibrils glide and functions as a support for traversing blood vessels, nerves, and lymphatic vessels (Schleips et al., 2012). Loose connective tissue rich in hyaluronic acid and with varying fiber directions acts as a buffer that enables the tissue to glide (Stecco et al., 2011). We hypothesized that when the elasticity of loose connective tissue of the myofascia has been changed pathologically, there is an associated decrease in the deformation of the skeletal muscle during joint motion and an increase in muscle hardness. However, no consensus standardized values of skeletal muscle deformation during joint motion have been established. Thus, skeletal deformation cannot be assessed effectively using US in the clinical setting. The vastus lateralis muscle (VL) originates at the lateral lip of the linea aspera of the femur and inserts at the tibial tubercle. The VL acts a strong extensor of the knee, and an increase in the hardness of the VL can lead to anterior knee pain syndrome such as patelofemoral joint arthritis and jumper’s knee. Therefore, evaluation of the hardness of the VL is important. However, this evaluation depends on palpation of the VL, which is not an objective method. No quantitative methods have been identified to evaluate the hardness of the VL. The aims of this study were to clarify the relationship between deformation of the VL during knee flexion and the hardness of the VL. Moreover the cut off value, which can assess decreased deformation of the VL, was estimated.
S. Kudo, S. Nakamura
Methods Forty lower limbs of 20 male normal volunteers participated in this study. All of the volunteers provided informed consent. The volunteers were divided into control and tightness groups using the Ely test. Twenty limbs of 10 subjects who showed a negative score on the Ely test were assigned to the control group, and the other 20 limbs of 10 subjects who showed a positive score on the Ely test were assigned to the tightness group. The Ely test was performed one time by a physical therapist who had 8years clinical experiences in orthopedics physical therapy. Positive Ely test was defined as the condition which could not be touched the own heel to the buttocks with keeping the bilateral anterior superior iliac spina contact to the bed in prone lying. General characteristics of all subjects are shown in Table 1. This study was approved by the ethics committee of our university. Deformation of the VL in the transverse plane during active knee flexion from 0 to 90 was recorded using Bmode US (Mylab25; Esaote, Indianapolis, IN, USA) with a 12 MHz liner probe fixed on the lateral side of the distal one third of the thigh by an original fixation device. Movement of the postero-lateral corner of the VL in the US image from 0 to 90 degrees of knee flexion was measured using Image-J (NIH) (Fig. 1). Deformation of the VL was measured 3 times, and the mean value was accepted. Hardness of the VL was measured using a durometer (TDM-NA1(DX) TRY-ALL INC., Japan) and a hand held dynamometer (mtus F-1, Anima co., Japan). For the durometer measurement, a single examiner performed 3 repetitions to measure the hardness on the middle lateral thigh in the supine position with the knee extended. In the torque meter measurement, the subject’s knee was fully flexed and held by a single examiner using a jig with a hand held dynamometer. Subjects were positioned as prone and relaxed and their pelvis and thigh were fixed on a bed using a hard polyester band. The axis of the jig was set on the knee joint axis, and the hand held dynamometer was set on the distal end of the leg. The reaction force at fully passive flexion, assessed by a single examiner, divided by the leg length was calculated, and the mean value of the reaction force over 5 repetitions was determined as the passive torque. The muscle tenderness at the lateral side of the middle thigh was evaluated by a single examiner using an algometer (FP meter, Matsumiya co., Japan). All parameters were measured in 3 repetitions, and the average of the 3 measurement values was accepted. All measurements were repeated 3 times to assess test-retest reliability (10
Table 1
General characteristic data.
Age (y/o) Height (cm) Weight (kg) BMI
All
Control group
Tightness group
P-value
20.0 2.3 167.4 5.8 59.9 6.9 20.4 2.4
19.1 0.9 170.4 6.4 57.2 7.3 19.6 2.3
20.1 2.4 167.4 6.1 59.9 7.3 21.4 2.3
0.23 0.22 0.42 0.1
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
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Relationship between hardness and deformation of the vastus lateralis
3
Figure 1 US image of the VL deformation. Postero-lateral corner of the VL was moved to postero-lateral direction during active knee flexion. (a; US image of the VL at 0 degree of knee. b; US image of the VL at 90 flexion of knee. VL; Vastus Lateralis. BF; Biceps Femoris. F: Femur. l; distance postero-lateral corner of the VL from 0 to 90 degree of the knee.)
healthy males; mean age, 21.2 2.1 y/o; mean height, 168.5 4.8 cm; mean weight, 58.4 6.9 kg). The muscle hardness, tenderness, passive torque, and deformation of the VL were compared between the 2 groups using the ManneWhitney test. The relationship between the deformation of the VL and the other 3 parameters were investigated using the Spearman correlation coefficient. Moreover, both the sensitivity and specificity of the morphological changes of the VL were calculated, and the ROC curve was drawn. Cut-off values were determined by the Yonden index. The reliability of the dynamics of the VL was examined using intraclass correlation coefficients (ICC), and the standard error of measurement (SEM) was calculated. All statistical methods were performed using R2.8.1 (free software).
of control group. However, the tenderness of the VL was not significantly different between the 2 groups. The correlation values between the deformation of the VL and the other parameters are shown in Table 3. The deformation of the VL showed a significantly higher correlation with hardness of the VL using the durometer, with significant mild correlation with passive torque in terminal knee flexion. However, there was no significant correlation between deformation of the VL and tenderness. The area of under the curve of the ROC curve concerning deformation of the VL was 0.9, and the cut-off value was 12.5 mm based on the Youden index. Both sensitivity and specificity of the cut off value were 0.95, respectively.
Discussion Results The ICC of the deformation of the VL was 0.92, and the SEM was 0.41 mm. The mean values of the passive torque, the deformation of the VL, the tenderness, and the hardness of both groups were shown in Table 2. The deformation of the VL of the tightness group was significantly decreased with that of control group. And hardness of the VL and passive torque of the tightness were significant smaller than those
Table 2 Difference of the parameter between control and tightness group.
Passive torque (N) Deformation of the VL (mm) Tenderness (kg) Hardness (N)
Control group
Tightness group
P-value
124.1 19.3 1.5 0.2
249.8 24.9 0.9 0.2
<0.001 <0.001
A high viscoelasticity of the skin, fascia, subcutaneous tissue (adipose tissue, dense and loose connective tissue), myofascia, and muscle is required during joint motion. The subcutaneous tissues help buffer the friction force (Stecco, 2015). Moreover, the intermuscular connective tissue mediates significant interactions between adjacent muscles (Huijing and Baan, 2001). The force between adjacent muscles may be influenced by the deformation of the muscle during motion through inter-muscular connective tissue. In the clinical setting, therapists perform muscle stretching for patients with restricted range of joint motion, in order to increase the elasticity of the skeletal
Table 3 Correlation of the deformation and the other parameter.
Deformation of the VL 4.4 0.5 34.6 1.8
4.5 0.9 42.3 3.2
0.61 <0.001
- Passive torque - Hardness - Tenderness
r
P-value
0.51 0.74 0.01
<0.001 <0.001 0.92
Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006
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4 muscle. However, the elasticity of skeletal muscle is due not only to muscle fascicles, but also to connective tissue around the skeletal muscle such as myofascia. The hardness of skeletal muscles is affected by surrounding structures. Therefore, it is important to assess the hardness of the connective tissue around the muscle. Recent studies highlight the connections of muscle with the dense connective tissue of the locomotor system, commonly referred to as fascia (Stecco et al., 2009; Huijing, 2009). Muscles can stretch the fascia in a longitudinal sense through expansions that stem from the tendons. They can also stretch fascia in a transversal sense through the intramuscular connective tissue (endomysium, perimysium, and epimysium) (Huijing and Jaspers, 2005; Purslow, 2010) and through the dense connective tissue of the musculoskeletal system (intermuscular septum, neurovascular bundles). However, the elasticity of those connective tissues cannot be measured using previously available methods. In this study, the tightness group identified using the Ely test showed significantly decreased muscle deformation of the VL and increased passive torque and hardness compared to that of the control group. Tenderness of pain was not significantly different between the 2 groups. These results suggest that the deformation of the VL observed during knee flexion using US correlates with the hardness of the VL. Moreover, the deformation of the VL showed a strong correlation with hardness assessed using a durometer, and showed a mild correlation with passive torque. The durometer measured muscle hardness through the skin and subcutaneous tissue. Therefore, the values obtained may not reflect only the hardness of the muscle (Ichilkawa et al., 2015), but also the hardness the skin and subcutaneous tissue. The passive torque of the muscle reflects predominately the elasticity of the muscle. Therefore, the deformation of the VL using US indicates the hardness of both the muscle and subcutaneous tissue around the muscle. Measurements of the deformation of the VL may be predicted by the elasticity around the VL. Increased hardness of the VL can lead to anterior knee pain syndrome. The Ely test in the clinical setting should be performed when the hardness of the VL is suspected. However, if patients have other impairments of the knee, such as osteoarthritis, the Ely test cannot be performed because the range of flexion of the knee is restricted. In these cases, dynamics of the VL are able to assess the flexibility of the VL quantitatively. The cut off value of the deformation of the VL was 12.5 mm. It can assess increasing hardness of the VL, when deformation of the VL was less than 12.5 mm. This study have two limitations. One is analysis of this study is a two dimensional analyses of muscle deformation, although the dynamics of the VL are shown as three dimensional movement in vivo. Therefore, deformation of the VL in this study was not defined by movements of identical points from 0 to 90 degrees of knee flexion, but was estimated from longitudinal changes during VL movement. Another is the Ely test is performed one time only. Ely test has a sensitivity ranging from 56 to 59% and the specificity ranging from 64 to 85% when assess the spasticity of the quadriceps in the cerebral palsy (Marks et al., 2003). However the Ely test is widely used methods which has high
S. Kudo, S. Nakamura reliability (Piva et al., 2006) for assessing the tightness of the quadriceps in the clinical setting. Therefore, decreasing deformation of the VL can be assessed the decreasing elasticity around the VL, although a processing that subjects are divided into two groups have a bias in this study.
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Please cite this article in press as: Kudo, S., Nakamura, S., Relationship between hardness and deformation of the vastus lateralis muscle during knee flexion using ultrasound imaging, Journal of Bodywork & Movement Therapies (2016), http://dx.doi.org/10.1016/ j.jbmt.2016.08.006