Journal of Applied Biomechanics, 2014, 30, 415-422 http://dx.doi.org/10.1123/jab.2013-0220 © 2014 Human Kinetics, Inc.
An Official Journal of ISB www.JAB-Journal.com ORIGINAL RESEARCH
Growth Changes in Morphological and Mechanical Properties of Human Patellar Tendon in Vivo Keitaro Kubo,1 Takanori Teshima,2 Norikazu Hirose,3 and Naoya Tsunoda2 1University
of Tokyo; 2Kokushikan University; 3Waseda University
The purpose of this study was to compare the morphological and mechanical properties of the human patellar tendon among elementary school children (prepubertal), junior high school students (pubertal), and adults. Twenty-one elementary school children, 18 junior high school students, and 22 adults participated in this study. The maximal strain, stiffness, Young’s modulus, hysteresis, and cross-sectional area of the patellar tendon were measured using ultrasonography. No significant difference was observed in the relative length (to thigh length) or cross-sectional area (to body mass2/3) of the patellar tendon among the three groups. Stiffness and Young’s modulus were significantly lower in elementary school children than in the other groups, while no significant differences were observed between junior high school students and adults. No significant differences were observed in maximal strain or hysteresis among the three groups. These results suggest that the material property (Young’s modulus) of the patellar tendons of elementary school children was lower than that of the other groups, whereas that of junior high school students was already similar to that of adults. In addition, no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups. Keywords: Young’s modulus, hysteresis, cross-sectional area, ultrasonography Many children are injured as a result of participation in strenuous activities and competitive sports.1,2 The injuries observed in growing children may reflect the growth characteristics of the immature skeleton.3,4 To date, few studies have ever attempted to investigate growth changes in human tendon properties in vivo, although changes in muscle strength and size have been demonstrated during growth.5–7 Previous studies have demonstrated that tendon structures were more compliant in children than in adults.8–10 We also reported that the knee extensor tendon properties of junior high school student (approximately 15 y) were already similar to those of adults.8 However, tendon-aponeurosis structures were investigated in two previous studies.8,10 Only one previous study attempted to compare the mechanical properties of the patellar tendon (outer tendon) in children and adults.9 However, the detailed method of tendon elongation for children (approximately 9 y) was not described in this study.9 Concerning the “accurate” position of the deep insertion of the patellar tendon on the tibial tuberosity for children, we need to identify the point of contact between the lower end of the patellar tendon and the growth plate (epiphyseal plate). A stress-strain relationship and Young’s modulus of tendon should be determined to accurately compare the mechanical properties of tendons between different age groups. However, tendonaponeurosis structures, but not the outer tendon, were investigated in previous studies by Kubo et al8 and Waugh et al,10 therefore, mateKeitaro Kubo is with the Department of Life Science, University of Tokyo, Meguro, Tokyo, Japan. Takanori Teshima is with the Department of Physical Education, Kokushikan University, Tokyo, Japan. Norikazu Hirose is with the Faculty of Sports Sciences, Waseda University, Tokorozawa, Saitama, Japan. Naoya Tsunoda is with the Department of Physical Education, Kokushikan University, Tokyo, Japan. Address author correspondence to Keitaro Kubo at [email protected].
rial properties (ie, Young’s modulus) have not yet been evaluated. According to the previous findings,9,10 the absolute tendon crosssectional area was smaller in children than in adults. However, we should note differences in physical characteristics (including height and body mass) when growth changes in the morphological properties (length and cross-sectional area) of tendons are investigated. Furthermore, Magnusson et al11 reported that the cross-sectional area of the Achilles tendon was greater in elderly women than in young women, which may reduce the risk of injury to the tendons of elderly people. Many previous studies have demonstrated that muscle size (ie, thickness, cross-sectional area) increases with growth5–7 and decreases with aging.12 Therefore, growth change in the size of tendons may be different from age-related changes in the size of muscles. In particular, the immature musculoskeletal system of children may be protected to reduce the imposed stress by an increased tendon size. Hysteresis of the tendon represents energy lost as heat due to internal damping, while the area under the unloading curve is the energy recovered in elastic recoil.13 Hence, hysteresis of the tendon should be considered when estimating the dynamics of the muscletendon complex during human movements. We previously reported that the difference in concentric torque with and without prior eccentric contractions (ie, prestretch augmentation) was negatively correlated with hysteresis of tendon structures.14 Moreover, recent studies showed that hysteresis of the tendon changed with aging, training, and immobilization.15–17 We previously demonstrated that hysteresis of the tendon structures in knee extensors increased with aging.16 This finding suggested that the dissipated elastic energy during stretch-shortening cycle exercises was greater in elderly people than in young people. Shadwick18 reported that hysteresis of the tendon was greater in newborn pigs than in mature pigs. If this finding is applied to human tendons in vivo, the lower running economy of children19,20 may be in part related to the greater hysteresis of the tendons in the lower limbs. Krahenbuhl and Williams19 415
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416 Kubo et al.
reported that younger children consumed more oxygen per kilogram of body mass than adults when running at the same speed. Therefore, elucidating growth changes in hysteresis of human tendon structures is important for clarifying the mechanism of growth changes in the performance during human movements. The morphological and mechanical properties of the patellar tendon were compared between children (approximately 9 y) and adults in only one previous study investigating growth changes in the outer tendon.9 However, it was not clear at which age the growth changes in the properties of the outer tendon begin, although the tendon-aponeurosis structures in knee extensors of junior high school student (approximately 15 y) were shown to be similar to those of adults.8 In the current study, we attempted to compare the morphological and mechanical properties of the human patellar tendon among elementary school children (prepubertal), junior high school students (pubertal), and adults. We hypothesized that the maximal strain, hysteresis, and relative cross-sectional area of the patellar tendon (outer tendon) would be greater in elementary school children than in adults, while those of junior high school students would be similar to those of adults.
Methods Subjects Twenty-one elementary school children (9.7–12.5 y), 18 junior high school students (13.0–14.8 y), and 22 young adults (19.4–26.2 y) participated in this study. All subjects were male. The ages and physical characteristics of each group are shown in Table 1. Taking the heights and body masses of elementary school children and junior high school students into account, it appears reasonable to assume that the subjects participating in this study were average Japanese upper grade elementary school children (approximately 11 y) and junior high school students (approximately 14 y).5,6 Adults were either sedentary, or mildly to moderately active men. Elementary school children and junior high school students were not involved in any specific physical training program beyond their normal school curriculum activities. The procedures, purpose, and risks associated with the study were explained to all subjects and their parents (for elementary school children and junior high school students) before they gave their written informed consent to participate in this investigation. The current study was approved by the Office of the Department of Sports Sciences, University of Tokyo, and complied with their requirements for human experimentation.
Morphological Properties of the Patellar Tendon
of the patellar tendon length (Figure 1). An outline of the tendon was traced from the axial image, and the traced image was transferred to a computer to calculate the cross-sectional area of the tendon using open-source image analysis software (Image J, NIH, Bethesda, MD). The length of patellar tendon was measured as the length from the apex of the patellar to the superior aspect of the tibial tuberosity.21 Concerning the “accurate” position of the deep insertion of the patellar tendon on the tibial tuberosity for elementary school children, we identified a point of contact between the lower end of the patellar tendon and the epiphyseal plate, as shown in Figure 2A.
Mechanical Properties of the Patellar Tendon The subject sat in a specially designed dynamometer (Applied Office, Tokyo, Japan) with support for the back and the hip joint was flexed at an angle of 80 deg (full extension = 0 deg) to standardize measurements and localize the action to the appropriate muscle group. The ankle was firmly attached to the lever arm of the dynamometer with a strap and fixed with the knee joint flexed at an angle of 90 deg. The center of rotation of the dynamometer was visually aligned with the center of rotation of the knee joint under submaximal contraction conditions. Before testing, each subject performed a standardized warm-up and submaximal contractions to become accustomed to the test procedure. Subjects were instructed to develop a gradually increasing force from a relaxed state to maximal voluntary contraction (MVC) within 5 s, followed by gradual relaxation within 5 s. The task was repeated two times per subject with at least three minutes between trials. The measured values that are shown below are the means of two trials. To estimate the coactivation level of the biceps femoris muscles, the integrated electromyographic activity of the biceps femoris muscles was measured during knee extension contraction. A maximal knee flexion isometric contraction was performed at the same angle (90 deg of the knee joint) to determine the maximal activation of the biceps femoris muscles. We normalized the integrated electromyographic activity value of biceps femoris muscles with respect to the integrated electromyographic activity value of biceps femoris muscles at the same angle when acting as an agonist at maximal effort. Assuming a linear relationship between the electromyographic activity value and torque, the antagonistic torque of the knee flexors (mainly biceps femoris muscles) during knee extension was calculated, and the addition of this torque to the measured knee extension torque produced the torque exerted by the knee extensors alone.22 The calculated knee joint torque (TQ) was converted to tendon force (Ft) by the following equation:
The cross-sectional area of the patellar tendon was measured using an ultrasonic apparatus (SSD-6500, Aloka, Tokyo, Japan) at 50%
Ft = TQ ∙ MA–1
Table 1 Age and physical characteristics of the subjects; mean (SE) Elementary School Children
Junior High School Students
Adults
Age (years)
11.2 (0.2)
13.8 (0.1)
22.3 (0.4)
*#
Height (cm)
141.9 (1.4)
163.0 (1.7)
170.6 (1.3)
*#
Body mass (kg)
33.8 (1.1)
49.0 (1.5)
68.4 (2.2)
*#
Thigh length (cm)
33.0 (0.4)
37.9 (0.4)
38.9 (0.3)
*
* Significant difference between elementary school children and the other two groups. # Significant difference between junior high school students and adults.
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Growth Changes in the Patellar Tendon 417
Figure 1 — Transverse ultrasonic image of the patellar tendon for an elementary school child (A) and adult (B).
where MA is the moment arm length of the patellar tendon at 90 deg of knee flexion for elementary school children (32 mm) and junior high school students and adults (40 mm).9 Stress was calculated as Ft per cross-sectional area of the patellar tendon. An ultrasonic apparatus with an 80 mm long probe (UST-5712, Aloka, Tokyo, Japan) was used to obtain longitudinal ultrasonic images of the patellar tendon. In the current study, elongation of the patellar tendon (L) was determined as a change in the distance between the tibia and distal apex of the patellar (Figure 2). As mentioned above (in Morphological Properties of the Patellar Tendon), we identified the point of contact (deep insertion of the patellar tendon) between the lower end of the patellar tendon and epiphyseal plate for elementary school children (Figure 2A). The strain of the patellar tendon was calculated as L values normalized to the tendon’s resting length (see above). To compare stiffness and Young’s modulus appropriately among subjects producing different forces, values were calculated in common force and stress regions.9 In the current study, 987–1410 N and 20.0–28.5 MPa, which corresponded to 70% and 100% MVC of the weakest elementary school child, were used to calculate stiffness and Young’s modulus. In addition, elastic energy absorption by the patellar tendon was proposed by calculating the area below the Ft – L curve from 0 to 100% MVC. The area within the Ft–L loop, as a percentage of the area beneath the curve during the ascending phase, was calculated as hysteresis.23
Statistics Values are reported as means ± standard error (SE). A one-way analysis of variance (ANOVA) was used for comparisons among the three groups. If the F statistic of the analysis of variance was significant, differences between groups were assessed by a Tukey post hoc test. The level of significance was set at P < .05.
Results Height and body mass were the highest in adults and lowest in elementary school children (Table 1). Thigh length was significantly lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults (P = .207) (Table 1). The dimension (length and cross-sectional area) of the patellar tendon increased in parallel with increases in body size. The absolute tendon length was significantly lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults (P = .282) (Table 2). The absolute cross-sectional area of the patellar tendon was the greatest in adults and the lowest in elementary school children. No significant difference was observed in the relative length (to thigh length) (P = .298) or cross-sectional area (to body mass2/3) (P = .481) of the patellar tendon among the three groups (Table 2).
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Figure 2 — Ultrasonic images of the longitudinal sections of the patellar tendon during an isometric contraction for an elementary school child (A) and adult (B).
Table 2 Morphological properties of the patellar tendon for the three groups; mean (SE) Elementary School Children
Junior High School Students
Adults
38.5 (0.8)
45.3 (0.6)
47.0 (0.8)
*
0.116 (0.002)
0.119 (0.002)
0.121 (0.002)
n.s.
49.2 (2.3)
65.4 (2.8)
82.7 (2.1)
*#
4.70 (0.17)
4.94 (0.25)
4.98 (0.12)
n.s.
Initial length (mm) Relative initial length to thigh length (mm∙mm–1) Cross-sectional area (mm2) Relative cross-sectional area (to body mass2/3) (mm∙kg–2/3)
* Significant difference between elementary school children and the other two groups. # Significant difference between junior high school students and adults.
418
Growth Changes in the Patellar Tendon 419
Table 3 Mechanical properties of the patellar tendon for the three groups; mean (SE)
Maximal elongation (mm)
Elementary School Children
Junior High School Students
Adults
2.81 (0.18)
3.06 (0.26)
3.84 (0.24)
§
Maximal strain (%)
7.94 (0.55)
7.03 (0.56)
8.19 (0.49)
n.s.
Stiffness (N∙mm–1)
742.9 (55.2)
1211.9 (136.0)
1507.2 (148.1)
*
Young’s modulus (MPa)
533.6 (36.1)
867.4 (65.5)
1039.0 (144.5)
*
Elastic energy (J)
2.49 (0.25)
4.30 (0.49)
8.77 (0.62)
#§
Hysteresis (%)
23.5 (1.9)
23.2 (2.5)
21.6 (2.9)
n.s.
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* Significant difference between elementary school children and the other two groups. # Significant difference between junior high school students and adults. § Significant difference between elementary school children and adults.
The material property (Young’s modulus) of elementary school children was lower than that of the other groups, while no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups. Stiffness and Young’s modulus were significantly lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults (P = .231 for stiffness, P = .478 for Young’s modulus) (Table 3, Figures 3 and 4). Elastic energy absorption by the patellar tendon was the highest in adults and lowest in elementary school children (Table 3). No significant differences were observed in the maximal strain (P = .133, Figure 4) or hysteresis (P = .787, Figure 5) among the three groups (Table 3).
Discussion The main findings of this study were that (1) the dimension (length and cross-sectional area) of the patellar tendon increased in parallel with increases in body size (limb length and body mass) during growth; (2) no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups; (3) the material property (Young’s modulus) of the patellar tendon was lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults. Young’s modulus was significantly lower in elementary school children than in adults. This result agreed with the finding of O’Brien et al.9 Previous studies using animal experiments also showed that the Young’s modulus of tendons increased during growth.18,24 For example, Shadwick18 reported that Young’s modulus increased from 0.16 GPa at birth to 1.6 GPa at maturity. According to these previous findings, however, it is not clear at which age this increase begins. In the current study, we found that Young’s modulus in junior high school students was already similar to that in adults. This result was supported by our previous finding on tendon-aponeurosis structures in the knee extensors.8 On the other hand, the relative MVC (to body mass) and muscle thickness (to body mass1/3) of junior high school students were still lower than those of adults (data not shown). Our previous study also demonstrated that age-related changes in the Achilles tendon, ie, decline in tendon extensibility, were already observed in men in their thirties, while no significant differences were observed in muscle strength or thickness between the 20- and 30-year-old groups.25 Considering these findings, the rates of alterations in tendons during growth and aging may be faster than those
of muscles. However, these discussions are speculative and await additional data for clarification. Growth changes in Young’s modulus of the tendon as mentioned above have been attributed to changes in size, namely, cross-sectional area and length. In the current study, the length and cross-sectional area of the patellar tendon increased in parallel with increases in body size (limb length and body mass) during growth. To date, a few studies have investigated growth changes in the size of tendons in vivo.9,10 In these studies,9,10 the absolute tendon cross-sectional area of children only was compared with that of adults. On the other hand, concerning age-related changes in tendon size, the cross-sectional area of the Achilles tendon was greater in elderly individuals than in young individuals,11 while no significant difference was observed in that of the patellar tendon between old and young men.26 Magnusson et al11 suggested that the larger Achilles tendon in elderly people may reduce the risk of injury to the tendon. More recently, we demonstrated that the relative cross-sectional area of the Achilles tendon was significantly larger in children than in adults.27 Considering these findings, we suggest that changes in tendon size during growth and aging differ between the patellar and Achilles tendons. Recent studies have shown that hysteresis of human tendons changes with aging, training, and immobilization.15–17 Hysteresis of the tendon represents energy lost as heat due to internal damping during stretch-shortening cycle exercises, such as jumping and running.13 According to previous findings,19,20 younger children consumed more oxygen per kilogram of body mass than adults when running at the same speed. The mechanisms for the lower running economy in children remain unclear, although physiological, biomechanical, and anatomical variables have been implicated.28 This lower running economy in children may be in part related to hysteresis of the tendon. However, to the best of our knowledge, no studies have investigated growth changes in hysteresis of the human tendon in vivo. According to the finding of an animal experiment,18 tendon hysteresis in the pig decreased during growth (24.5% in newborn and 9.2% in mature). Although we previously hypothesized that hysteresis was greater in children than in adults, this was rejected by the current study. Finni et al29 recently reported that hysteresis values from human studies in vivo were greater than those from animal studies in vitro,30,31 and that there was a very large range of hysteresis values for humans.14–16 They explained that these issues may have been due to the difficulty in controlling the relaxation phase and a low sampling frequency of ultrasound images. A more reliable technique to measure hysteresis of the human tendon in vivo is required in future studies to understand growth changes in hysteresis of the human tendon.
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420 Kubo et al.
Figure 3 — Relationship between the estimated tendon force (Ft) and elongation of the tendon (L) for elementary school children (open square), junior high school students (closed rhombus), and adults (open cross).
Figure 4 — Relationship between the estimated tendon stress and strain for elementary school children (open square), junior high school students (closed rhombus), and adults (open cross).
Figure 5 — %MVC: elongation (L) of the patellar tendon during the ascending (open square) and descending (closed circle) phases produced a loop for elementary school children (A), junior high school students (B), and adults (C).
The average maximal strain of the patellar tendon was approximately 8% for the three age groups, which was consistent with those reported previously in vivo.9,32–34 However, O’Brien et al9 reported that the maximal strain of boys (about 18%) was markedly greater than that of adult men (about 8%) according to their Figure 4. This result on the maximal strain of boys was not consistent with our present result. Unfortunately, the reason for this discrepancy remains unknown. A detailed method for tendon elongation for boys was not described in O’Brien et al.9 As mentioned above in Methods, in the subsections on the morphological and mechanical properties of the patellar tendon, we identified a point of contact (deep insertion of the patellar tendon on the tibial tuberosity) for elementary school children between the lower end of the patellar tendon and the epiphyseal plate, as shown in Figure 2A. Therefore, we considered that the length and elongation of the patellar tendon for elementary school children were measured accurately. In the current study, we must draw the attention to the limitations and assumptions of the methodology followed. Firstly, we
used a previously reported moment arm length in each age group to calculate the tendon force.9 In most previous studies on human tendon properties,35 the moment arm length has been estimated from the limb length.36,37 However, Tsaopoulos et al38 demonstrated that the moment arm length of the patellar tendon was not able to be predicted from several externally measured anthropometric characteristics, namely, limb length. Furthermore, the moment arm length was previously reported to change with increasing muscle force.39,40 Therefore, it is difficult to obtain accurate moment arm lengths during the measurement of tendon properties. We cannot rule out that variations in the moment arm length among subjects may have influenced the calculated tendon force and Young’s modulus. We considered that this point did not affect the other measured variables (including maximal strain and hysteresis) in the current study. Secondly, this is a cross-sectional study with no control for biological maturation or historical background. Unfortunately, we could not control the historical background of each subject. Concerning the biological maturation of elementary school children
Growth Changes in the Patellar Tendon 421
and junior high school students, the heights and body masses of elementary school children and junior high school students were similar to previously reported values.5,6 Therefore, we considered our subjects to be average Japanese upper grade elementary school children (approximately 11 y) and junior high school students (approximately 14 y). In conclusion, the material property (Young’s modulus) of the patellar tendon was lower in elementary school children than in the other groups, while that of junior high school students was already similar to that of adults. In addition, no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups.
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Acknowledgments This study was supported by a Grant-in-Aid for Young Scientists (A) (21680047 to K. Kubo) from Japan Society for the Promotion of Science. The authors would like to thank Mr. Shinkawa K. and Mr. Ohkawa M. for their conscientious work in this project and the subjects and their parents who participated in this study.
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13. Butler DL, Grood ES, Noyes FK, Zernicke RF. Biomechanics of ligaments and tendons. In: R.S. Hutton (ed). Exercise and Sport Sciences Reviews. 1978;125–181. 14. Kubo K, Kanehisa H, Fukunaga T. Effects of viscoelastic properties of tendon structures on stretch-shortening cycle exercises in vivo. J Sports Sci. 2005;23:851–860. PubMed doi:10.1080/02640410400022029 15. Fouré A, Nordez A, Cornu C. Plyometric training effects on Achilles tendon stiffness and dissipative properties. J Appl Physiol. 2010;109:849–854. PubMed doi:10.1152/japplphysiol.01150.2009 16. Kubo K, Kanehisa H, Miyatani M, Tachi M, Fukunaga T. Effect of low-load resistance training on the tendon properties in middle aged and elderly women. Acta Physiol Scand. 2003;178:25–32. PubMed doi:10.1046/j.1365-201X.2003.01097.x 17. Reeves ND, Maganaris CN, Ferretti G, Narici MV. Influence of 90-day simulated microgravity on human tendon mechanical properties and effect of resistive countermeasures. J Appl Physiol. 2005;98:2278– 2286. PubMed doi:10.1152/japplphysiol.01266.2004 18. Shadwick RE. Elastic energy storage in tendons: mechanical differences related to function and age. J Appl Physiol. 1990;68:1033–1040. PubMed 19. Krahenbuhl GS, Williams TJ. Running economy: changes with age during childhood and adolescence. Med Sci Sports Exerc. 1992;24:462–466. PubMed doi:10.1249/00005768-199204000-00012 20. MacDougall JD, Roche PD, Bar-Or O, Moroz J. Maximal aerobic capacity of Canadian school children: prediction based on age-related oxygen cost of running. Int J Sports Med. 1983;4:194–198. PubMed doi:10.1055/s-2008-1026034 21. Hansen P, Bojsen-Moller J, Aagaard P, Kjaer M, Magnusson SP. Mechanical properties of the human patellar tendon, in vivo. Clin Biomech (Bristol, Avon). 2006;21:54–58. PubMed doi:10.1016/j. clinbiomech.2005.07.008 22. Magnusson SP, Aagaard P, Rosager S, Poulsen PD, Kjaer M. Loaddisplacement properties of the human triceps surae aponeurosis in vivo. J Physiol. 2001;531:277–288. PubMed doi:10.1111/j.14697793.2001.0277j.x 23. Kubo K, Kanehisa H, Fukunaga T. Effects of resistance and stretching training programs on the viscoelastic properties of tendon structures in vivo. J Physiol. 2002;538:219–226. PubMed doi:10.1113/ jphysiol.2001.012703 24. Nakagawa Y, Hayashi K, Yamamoto N, Nagashima K. Age-related changes in biomechanical properties of the Achilles tendon in rabbits. Eur J Appl Physiol. 1996;73:7–10. PubMed doi:10.1007/BF00262803 25. Kubo K, Morimoto M, Komuro T, Tsunoda N, Kanehisa H, Fukunaga T. Age-related differences in neuromuscular and mechanical properties of the plantar flexor muscles and tendon in untrained men. Med Sci Sports Exerc. 2007;39:541–547. PubMed doi:10.1249/01. mss.0000247006.24965.74 26. Couppé C, Hansen P, Kongsgaard M, et al. Mechanical properties and collagen cross-linking of the patellar tendon in old and young men. J Appl Physiol. 2009;107:880–886. PubMed doi:10.1152/japplphysiol.00291.2009 27. Kubo K, Teshima T, Hirose N, Tsunoda N. A cross-sectional study of the plantar flexor muscle and tendon during growth. Int J Sports Med. 2014, in press. PubMed doi:10.1055/s-0034-1367011 28. Frederick E. Synthesis, experimentation and the biomechanics of economical movement. Med Sci Sports Exerc. 1985;17:44–47. PubMed doi:10.1249/00005768-198502000-00008 29. Finni T, Peltonen J, Stenroth L, Cronin NJ. Viewpoint: On the hysteresis in the human Achilles tendon. J Appl Physiol. 2013;114:515–517. PubMed doi:10.1152/japplphysiol.01005.2012 30. Ker RF. Dynamic tensile properties of the plantaris tendon sheep (Ovis Aries). J Exp Biol. 1981;93:283–302. PubMed
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422 Kubo et al. 31. Pollock CM, Shadwick RE. Relationship between body mass and biomechanical properties of limb tendons in adult mammals. Am J Physiol Regul Integr Comp Physiol. 1994;266:R1016–R1021. PubMed 32. de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV. Time course of muscular, neural and tendinous adaptations to 23day unilateral lower-limb suspension in young men. J Physiol. 2007;583:1079–1091. PubMed doi:10.1113/jphysiol.2007.135392 33. Kubo K, Kanehisa H, Fukunaga T. Comparison of elasticity of human tendon and aponeurosis in knee extensors and ankle plantar flexors in vivo. J Appl Biomech. 2005;21:129–142. PubMed 34. Seynnes OR, Erskine RM, Maganaris CN, et al. Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol. 2009;107:523–530. PubMed doi:10.1152/japplphysiol.00213.2009 35. Kubo K, Tabata T, Ikebukuro T, Igarashi K, Yata H, Tsunoda N. Effects of mechanical properties of muscle and tendon on performance in long distance runners. Eur J Appl Physiol. 2010;110:507–514. PubMed doi:10.1007/s00421-010-1528-1
36. Greive DW, Pheasant S, Cavanagh PR. Prediction of gastrocnemius length from knee and ankle joint posture. In E. Asmussen and K. Jorgensen (eds), Biomechanics VI-A. 1978;405–412. 37. Visser JJ, Hoogkamer JE, Bobbert MF, Huijing PA. Length and moment arm of human leg muscles as a function of knee and hip-joint angles. Eur J Appl Physiol. 1990;61:453–460. PubMed doi:10.1007/ BF00236067 38. Tsaopoulos DE, Maganaris CN, Baltzopoulos V. Can the patellar moment arm be predicted from anthropometric measurements? J Biomech. 2007;40:645–651. PubMed doi:10.1016/j.jbiomech.2006.01.022 39. Ito M, Akima H, Fukunaga T. In vivo moment arm determination using B-mode ultrasonography. J Biomech. 2000;33:215–218. PubMed doi:10.1016/S0021-9290(99)00154-2 40. Tsaopoulos DE, Baltzopoulos V, Richards PJ, Maganaris CN. In vivo changes in the human patellar tendon moment arm length with different modes and intensities of muscle contraction. J Biomech. 2007;40:3325–3332. PubMed doi:10.1016/j.jbiomech.2007.05.005
An Official Journal of ISB www.JAB-Journal.com ORIGINAL RESEARCH
Growth Changes in Morphological and Mechanical Properties of Human Patellar Tendon in Vivo Keitaro Kubo,1 Takanori Teshima,2 Norikazu Hirose,3 and Naoya Tsunoda2 1University
of Tokyo; 2Kokushikan University; 3Waseda University
The purpose of this study was to compare the morphological and mechanical properties of the human patellar tendon among elementary school children (prepubertal), junior high school students (pubertal), and adults. Twenty-one elementary school children, 18 junior high school students, and 22 adults participated in this study. The maximal strain, stiffness, Young’s modulus, hysteresis, and cross-sectional area of the patellar tendon were measured using ultrasonography. No significant difference was observed in the relative length (to thigh length) or cross-sectional area (to body mass2/3) of the patellar tendon among the three groups. Stiffness and Young’s modulus were significantly lower in elementary school children than in the other groups, while no significant differences were observed between junior high school students and adults. No significant differences were observed in maximal strain or hysteresis among the three groups. These results suggest that the material property (Young’s modulus) of the patellar tendons of elementary school children was lower than that of the other groups, whereas that of junior high school students was already similar to that of adults. In addition, no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups. Keywords: Young’s modulus, hysteresis, cross-sectional area, ultrasonography Many children are injured as a result of participation in strenuous activities and competitive sports.1,2 The injuries observed in growing children may reflect the growth characteristics of the immature skeleton.3,4 To date, few studies have ever attempted to investigate growth changes in human tendon properties in vivo, although changes in muscle strength and size have been demonstrated during growth.5–7 Previous studies have demonstrated that tendon structures were more compliant in children than in adults.8–10 We also reported that the knee extensor tendon properties of junior high school student (approximately 15 y) were already similar to those of adults.8 However, tendon-aponeurosis structures were investigated in two previous studies.8,10 Only one previous study attempted to compare the mechanical properties of the patellar tendon (outer tendon) in children and adults.9 However, the detailed method of tendon elongation for children (approximately 9 y) was not described in this study.9 Concerning the “accurate” position of the deep insertion of the patellar tendon on the tibial tuberosity for children, we need to identify the point of contact between the lower end of the patellar tendon and the growth plate (epiphyseal plate). A stress-strain relationship and Young’s modulus of tendon should be determined to accurately compare the mechanical properties of tendons between different age groups. However, tendonaponeurosis structures, but not the outer tendon, were investigated in previous studies by Kubo et al8 and Waugh et al,10 therefore, mateKeitaro Kubo is with the Department of Life Science, University of Tokyo, Meguro, Tokyo, Japan. Takanori Teshima is with the Department of Physical Education, Kokushikan University, Tokyo, Japan. Norikazu Hirose is with the Faculty of Sports Sciences, Waseda University, Tokorozawa, Saitama, Japan. Naoya Tsunoda is with the Department of Physical Education, Kokushikan University, Tokyo, Japan. Address author correspondence to Keitaro Kubo at [email protected].
rial properties (ie, Young’s modulus) have not yet been evaluated. According to the previous findings,9,10 the absolute tendon crosssectional area was smaller in children than in adults. However, we should note differences in physical characteristics (including height and body mass) when growth changes in the morphological properties (length and cross-sectional area) of tendons are investigated. Furthermore, Magnusson et al11 reported that the cross-sectional area of the Achilles tendon was greater in elderly women than in young women, which may reduce the risk of injury to the tendons of elderly people. Many previous studies have demonstrated that muscle size (ie, thickness, cross-sectional area) increases with growth5–7 and decreases with aging.12 Therefore, growth change in the size of tendons may be different from age-related changes in the size of muscles. In particular, the immature musculoskeletal system of children may be protected to reduce the imposed stress by an increased tendon size. Hysteresis of the tendon represents energy lost as heat due to internal damping, while the area under the unloading curve is the energy recovered in elastic recoil.13 Hence, hysteresis of the tendon should be considered when estimating the dynamics of the muscletendon complex during human movements. We previously reported that the difference in concentric torque with and without prior eccentric contractions (ie, prestretch augmentation) was negatively correlated with hysteresis of tendon structures.14 Moreover, recent studies showed that hysteresis of the tendon changed with aging, training, and immobilization.15–17 We previously demonstrated that hysteresis of the tendon structures in knee extensors increased with aging.16 This finding suggested that the dissipated elastic energy during stretch-shortening cycle exercises was greater in elderly people than in young people. Shadwick18 reported that hysteresis of the tendon was greater in newborn pigs than in mature pigs. If this finding is applied to human tendons in vivo, the lower running economy of children19,20 may be in part related to the greater hysteresis of the tendons in the lower limbs. Krahenbuhl and Williams19 415
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416 Kubo et al.
reported that younger children consumed more oxygen per kilogram of body mass than adults when running at the same speed. Therefore, elucidating growth changes in hysteresis of human tendon structures is important for clarifying the mechanism of growth changes in the performance during human movements. The morphological and mechanical properties of the patellar tendon were compared between children (approximately 9 y) and adults in only one previous study investigating growth changes in the outer tendon.9 However, it was not clear at which age the growth changes in the properties of the outer tendon begin, although the tendon-aponeurosis structures in knee extensors of junior high school student (approximately 15 y) were shown to be similar to those of adults.8 In the current study, we attempted to compare the morphological and mechanical properties of the human patellar tendon among elementary school children (prepubertal), junior high school students (pubertal), and adults. We hypothesized that the maximal strain, hysteresis, and relative cross-sectional area of the patellar tendon (outer tendon) would be greater in elementary school children than in adults, while those of junior high school students would be similar to those of adults.
Methods Subjects Twenty-one elementary school children (9.7–12.5 y), 18 junior high school students (13.0–14.8 y), and 22 young adults (19.4–26.2 y) participated in this study. All subjects were male. The ages and physical characteristics of each group are shown in Table 1. Taking the heights and body masses of elementary school children and junior high school students into account, it appears reasonable to assume that the subjects participating in this study were average Japanese upper grade elementary school children (approximately 11 y) and junior high school students (approximately 14 y).5,6 Adults were either sedentary, or mildly to moderately active men. Elementary school children and junior high school students were not involved in any specific physical training program beyond their normal school curriculum activities. The procedures, purpose, and risks associated with the study were explained to all subjects and their parents (for elementary school children and junior high school students) before they gave their written informed consent to participate in this investigation. The current study was approved by the Office of the Department of Sports Sciences, University of Tokyo, and complied with their requirements for human experimentation.
Morphological Properties of the Patellar Tendon
of the patellar tendon length (Figure 1). An outline of the tendon was traced from the axial image, and the traced image was transferred to a computer to calculate the cross-sectional area of the tendon using open-source image analysis software (Image J, NIH, Bethesda, MD). The length of patellar tendon was measured as the length from the apex of the patellar to the superior aspect of the tibial tuberosity.21 Concerning the “accurate” position of the deep insertion of the patellar tendon on the tibial tuberosity for elementary school children, we identified a point of contact between the lower end of the patellar tendon and the epiphyseal plate, as shown in Figure 2A.
Mechanical Properties of the Patellar Tendon The subject sat in a specially designed dynamometer (Applied Office, Tokyo, Japan) with support for the back and the hip joint was flexed at an angle of 80 deg (full extension = 0 deg) to standardize measurements and localize the action to the appropriate muscle group. The ankle was firmly attached to the lever arm of the dynamometer with a strap and fixed with the knee joint flexed at an angle of 90 deg. The center of rotation of the dynamometer was visually aligned with the center of rotation of the knee joint under submaximal contraction conditions. Before testing, each subject performed a standardized warm-up and submaximal contractions to become accustomed to the test procedure. Subjects were instructed to develop a gradually increasing force from a relaxed state to maximal voluntary contraction (MVC) within 5 s, followed by gradual relaxation within 5 s. The task was repeated two times per subject with at least three minutes between trials. The measured values that are shown below are the means of two trials. To estimate the coactivation level of the biceps femoris muscles, the integrated electromyographic activity of the biceps femoris muscles was measured during knee extension contraction. A maximal knee flexion isometric contraction was performed at the same angle (90 deg of the knee joint) to determine the maximal activation of the biceps femoris muscles. We normalized the integrated electromyographic activity value of biceps femoris muscles with respect to the integrated electromyographic activity value of biceps femoris muscles at the same angle when acting as an agonist at maximal effort. Assuming a linear relationship between the electromyographic activity value and torque, the antagonistic torque of the knee flexors (mainly biceps femoris muscles) during knee extension was calculated, and the addition of this torque to the measured knee extension torque produced the torque exerted by the knee extensors alone.22 The calculated knee joint torque (TQ) was converted to tendon force (Ft) by the following equation:
The cross-sectional area of the patellar tendon was measured using an ultrasonic apparatus (SSD-6500, Aloka, Tokyo, Japan) at 50%
Ft = TQ ∙ MA–1
Table 1 Age and physical characteristics of the subjects; mean (SE) Elementary School Children
Junior High School Students
Adults
Age (years)
11.2 (0.2)
13.8 (0.1)
22.3 (0.4)
*#
Height (cm)
141.9 (1.4)
163.0 (1.7)
170.6 (1.3)
*#
Body mass (kg)
33.8 (1.1)
49.0 (1.5)
68.4 (2.2)
*#
Thigh length (cm)
33.0 (0.4)
37.9 (0.4)
38.9 (0.3)
*
* Significant difference between elementary school children and the other two groups. # Significant difference between junior high school students and adults.
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Growth Changes in the Patellar Tendon 417
Figure 1 — Transverse ultrasonic image of the patellar tendon for an elementary school child (A) and adult (B).
where MA is the moment arm length of the patellar tendon at 90 deg of knee flexion for elementary school children (32 mm) and junior high school students and adults (40 mm).9 Stress was calculated as Ft per cross-sectional area of the patellar tendon. An ultrasonic apparatus with an 80 mm long probe (UST-5712, Aloka, Tokyo, Japan) was used to obtain longitudinal ultrasonic images of the patellar tendon. In the current study, elongation of the patellar tendon (L) was determined as a change in the distance between the tibia and distal apex of the patellar (Figure 2). As mentioned above (in Morphological Properties of the Patellar Tendon), we identified the point of contact (deep insertion of the patellar tendon) between the lower end of the patellar tendon and epiphyseal plate for elementary school children (Figure 2A). The strain of the patellar tendon was calculated as L values normalized to the tendon’s resting length (see above). To compare stiffness and Young’s modulus appropriately among subjects producing different forces, values were calculated in common force and stress regions.9 In the current study, 987–1410 N and 20.0–28.5 MPa, which corresponded to 70% and 100% MVC of the weakest elementary school child, were used to calculate stiffness and Young’s modulus. In addition, elastic energy absorption by the patellar tendon was proposed by calculating the area below the Ft – L curve from 0 to 100% MVC. The area within the Ft–L loop, as a percentage of the area beneath the curve during the ascending phase, was calculated as hysteresis.23
Statistics Values are reported as means ± standard error (SE). A one-way analysis of variance (ANOVA) was used for comparisons among the three groups. If the F statistic of the analysis of variance was significant, differences between groups were assessed by a Tukey post hoc test. The level of significance was set at P < .05.
Results Height and body mass were the highest in adults and lowest in elementary school children (Table 1). Thigh length was significantly lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults (P = .207) (Table 1). The dimension (length and cross-sectional area) of the patellar tendon increased in parallel with increases in body size. The absolute tendon length was significantly lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults (P = .282) (Table 2). The absolute cross-sectional area of the patellar tendon was the greatest in adults and the lowest in elementary school children. No significant difference was observed in the relative length (to thigh length) (P = .298) or cross-sectional area (to body mass2/3) (P = .481) of the patellar tendon among the three groups (Table 2).
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Figure 2 — Ultrasonic images of the longitudinal sections of the patellar tendon during an isometric contraction for an elementary school child (A) and adult (B).
Table 2 Morphological properties of the patellar tendon for the three groups; mean (SE) Elementary School Children
Junior High School Students
Adults
38.5 (0.8)
45.3 (0.6)
47.0 (0.8)
*
0.116 (0.002)
0.119 (0.002)
0.121 (0.002)
n.s.
49.2 (2.3)
65.4 (2.8)
82.7 (2.1)
*#
4.70 (0.17)
4.94 (0.25)
4.98 (0.12)
n.s.
Initial length (mm) Relative initial length to thigh length (mm∙mm–1) Cross-sectional area (mm2) Relative cross-sectional area (to body mass2/3) (mm∙kg–2/3)
* Significant difference between elementary school children and the other two groups. # Significant difference between junior high school students and adults.
418
Growth Changes in the Patellar Tendon 419
Table 3 Mechanical properties of the patellar tendon for the three groups; mean (SE)
Maximal elongation (mm)
Elementary School Children
Junior High School Students
Adults
2.81 (0.18)
3.06 (0.26)
3.84 (0.24)
§
Maximal strain (%)
7.94 (0.55)
7.03 (0.56)
8.19 (0.49)
n.s.
Stiffness (N∙mm–1)
742.9 (55.2)
1211.9 (136.0)
1507.2 (148.1)
*
Young’s modulus (MPa)
533.6 (36.1)
867.4 (65.5)
1039.0 (144.5)
*
Elastic energy (J)
2.49 (0.25)
4.30 (0.49)
8.77 (0.62)
#§
Hysteresis (%)
23.5 (1.9)
23.2 (2.5)
21.6 (2.9)
n.s.
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* Significant difference between elementary school children and the other two groups. # Significant difference between junior high school students and adults. § Significant difference between elementary school children and adults.
The material property (Young’s modulus) of elementary school children was lower than that of the other groups, while no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups. Stiffness and Young’s modulus were significantly lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults (P = .231 for stiffness, P = .478 for Young’s modulus) (Table 3, Figures 3 and 4). Elastic energy absorption by the patellar tendon was the highest in adults and lowest in elementary school children (Table 3). No significant differences were observed in the maximal strain (P = .133, Figure 4) or hysteresis (P = .787, Figure 5) among the three groups (Table 3).
Discussion The main findings of this study were that (1) the dimension (length and cross-sectional area) of the patellar tendon increased in parallel with increases in body size (limb length and body mass) during growth; (2) no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups; (3) the material property (Young’s modulus) of the patellar tendon was lower in elementary school children than in the other groups, while no significant difference was observed between junior high school students and adults. Young’s modulus was significantly lower in elementary school children than in adults. This result agreed with the finding of O’Brien et al.9 Previous studies using animal experiments also showed that the Young’s modulus of tendons increased during growth.18,24 For example, Shadwick18 reported that Young’s modulus increased from 0.16 GPa at birth to 1.6 GPa at maturity. According to these previous findings, however, it is not clear at which age this increase begins. In the current study, we found that Young’s modulus in junior high school students was already similar to that in adults. This result was supported by our previous finding on tendon-aponeurosis structures in the knee extensors.8 On the other hand, the relative MVC (to body mass) and muscle thickness (to body mass1/3) of junior high school students were still lower than those of adults (data not shown). Our previous study also demonstrated that age-related changes in the Achilles tendon, ie, decline in tendon extensibility, were already observed in men in their thirties, while no significant differences were observed in muscle strength or thickness between the 20- and 30-year-old groups.25 Considering these findings, the rates of alterations in tendons during growth and aging may be faster than those
of muscles. However, these discussions are speculative and await additional data for clarification. Growth changes in Young’s modulus of the tendon as mentioned above have been attributed to changes in size, namely, cross-sectional area and length. In the current study, the length and cross-sectional area of the patellar tendon increased in parallel with increases in body size (limb length and body mass) during growth. To date, a few studies have investigated growth changes in the size of tendons in vivo.9,10 In these studies,9,10 the absolute tendon cross-sectional area of children only was compared with that of adults. On the other hand, concerning age-related changes in tendon size, the cross-sectional area of the Achilles tendon was greater in elderly individuals than in young individuals,11 while no significant difference was observed in that of the patellar tendon between old and young men.26 Magnusson et al11 suggested that the larger Achilles tendon in elderly people may reduce the risk of injury to the tendon. More recently, we demonstrated that the relative cross-sectional area of the Achilles tendon was significantly larger in children than in adults.27 Considering these findings, we suggest that changes in tendon size during growth and aging differ between the patellar and Achilles tendons. Recent studies have shown that hysteresis of human tendons changes with aging, training, and immobilization.15–17 Hysteresis of the tendon represents energy lost as heat due to internal damping during stretch-shortening cycle exercises, such as jumping and running.13 According to previous findings,19,20 younger children consumed more oxygen per kilogram of body mass than adults when running at the same speed. The mechanisms for the lower running economy in children remain unclear, although physiological, biomechanical, and anatomical variables have been implicated.28 This lower running economy in children may be in part related to hysteresis of the tendon. However, to the best of our knowledge, no studies have investigated growth changes in hysteresis of the human tendon in vivo. According to the finding of an animal experiment,18 tendon hysteresis in the pig decreased during growth (24.5% in newborn and 9.2% in mature). Although we previously hypothesized that hysteresis was greater in children than in adults, this was rejected by the current study. Finni et al29 recently reported that hysteresis values from human studies in vivo were greater than those from animal studies in vitro,30,31 and that there was a very large range of hysteresis values for humans.14–16 They explained that these issues may have been due to the difficulty in controlling the relaxation phase and a low sampling frequency of ultrasound images. A more reliable technique to measure hysteresis of the human tendon in vivo is required in future studies to understand growth changes in hysteresis of the human tendon.
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420 Kubo et al.
Figure 3 — Relationship between the estimated tendon force (Ft) and elongation of the tendon (L) for elementary school children (open square), junior high school students (closed rhombus), and adults (open cross).
Figure 4 — Relationship between the estimated tendon stress and strain for elementary school children (open square), junior high school students (closed rhombus), and adults (open cross).
Figure 5 — %MVC: elongation (L) of the patellar tendon during the ascending (open square) and descending (closed circle) phases produced a loop for elementary school children (A), junior high school students (B), and adults (C).
The average maximal strain of the patellar tendon was approximately 8% for the three age groups, which was consistent with those reported previously in vivo.9,32–34 However, O’Brien et al9 reported that the maximal strain of boys (about 18%) was markedly greater than that of adult men (about 8%) according to their Figure 4. This result on the maximal strain of boys was not consistent with our present result. Unfortunately, the reason for this discrepancy remains unknown. A detailed method for tendon elongation for boys was not described in O’Brien et al.9 As mentioned above in Methods, in the subsections on the morphological and mechanical properties of the patellar tendon, we identified a point of contact (deep insertion of the patellar tendon on the tibial tuberosity) for elementary school children between the lower end of the patellar tendon and the epiphyseal plate, as shown in Figure 2A. Therefore, we considered that the length and elongation of the patellar tendon for elementary school children were measured accurately. In the current study, we must draw the attention to the limitations and assumptions of the methodology followed. Firstly, we
used a previously reported moment arm length in each age group to calculate the tendon force.9 In most previous studies on human tendon properties,35 the moment arm length has been estimated from the limb length.36,37 However, Tsaopoulos et al38 demonstrated that the moment arm length of the patellar tendon was not able to be predicted from several externally measured anthropometric characteristics, namely, limb length. Furthermore, the moment arm length was previously reported to change with increasing muscle force.39,40 Therefore, it is difficult to obtain accurate moment arm lengths during the measurement of tendon properties. We cannot rule out that variations in the moment arm length among subjects may have influenced the calculated tendon force and Young’s modulus. We considered that this point did not affect the other measured variables (including maximal strain and hysteresis) in the current study. Secondly, this is a cross-sectional study with no control for biological maturation or historical background. Unfortunately, we could not control the historical background of each subject. Concerning the biological maturation of elementary school children
Growth Changes in the Patellar Tendon 421
and junior high school students, the heights and body masses of elementary school children and junior high school students were similar to previously reported values.5,6 Therefore, we considered our subjects to be average Japanese upper grade elementary school children (approximately 11 y) and junior high school students (approximately 14 y). In conclusion, the material property (Young’s modulus) of the patellar tendon was lower in elementary school children than in the other groups, while that of junior high school students was already similar to that of adults. In addition, no significant differences were observed in the extensibility (maximal strain) or viscosity (hysteresis) of the patellar tendon among the three groups.
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Acknowledgments This study was supported by a Grant-in-Aid for Young Scientists (A) (21680047 to K. Kubo) from Japan Society for the Promotion of Science. The authors would like to thank Mr. Shinkawa K. and Mr. Ohkawa M. for their conscientious work in this project and the subjects and their parents who participated in this study.
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