The Knee 32 (2021) 140–147

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Muscle stiffness of the rectus femoris and vastus lateralis in

children with Osgood–Schlatter disease
Shota Enomoto a,b,⇑, Toshiaki Oda c, Norihide Sugisaki a, Misaki Toeda d, Sadao Kurokawa a,
Masaru Kaga e
a
Center for Liberal Arts, Meiji Gakuin University, Yokohama, Japan
b
Joint Graduate School in Science of School Education, Hyogo University of Teacher Education, Hyogo, Japan
c
Graduate School of Education, Hyogo University of Teacher Education, Hyogo, Japan
d
Department of Clothing, Faculty of Human sciences and Design, Japan Women’s University, Tokyo, Japan
e
Graduate School of Education, Okayama University, Okayama, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Background: The relevance of the mechanical properties of muscles in relation to Osgood–
Received 23 February 2021 Schlatter disease (OSD) remains unclear. The present study aimed to examine rectus
Revised 8 June 2021 femoris (RF) and vastus lateralis (VL) muscle stiffness in children with OSD.
Accepted 4 August 2021
Methods: A total of 28 legs affected by OSD and 26 legs without OSD were assessed. The
shear-wave velocity (SWV) of the RF and VL (in m/s) during passive knee flexion (0° (i.e.,
fully extended position), 45°, and 90° knee joint flexion) and isometric contraction (50%
Keywords:
of maximal voluntary contraction) was measured using shear-wave elastography.
Elastography
Ultrasound
Results: The SWV of the RF was higher in subjects with OSD than in those without OSD at
Quadriceps femoris 45° and 90° flexion (P = 0.033 and P = 0.035, respectively); however, the SWV of the RF did
Associated factor not significantly differ at 0° flexion (P = 0.469). Similarly, the SWV of the VL exhibited no
Tibial tuberosity significant difference between the tested groups (P > 0.05). No significant difference in the
SWV of both muscles during isometric contraction was observed between the two groups
(P > 0.05).
Conclusions: The results suggest that a stiffer RF under stretched conditions (45° and 90°
flexion) is related to the presence of OSD. Furthermore, both muscles under unstretched
and contracted conditions and the VL under stretched conditions have limited association
with the presence of OSD. These results have important implications for understanding the
association between the mechanical properties of muscles and OSD.
Ó 2021 Elsevier B.V. All rights reserved.

1. Introduction

Osgood–Schlatter disease (OSD) is a condition characterized by traction apophysitis of the tibial tubercle and is common
in the active young population [1–3]. Increased quadriceps femoris muscle tightness based on the range of motion (ROM) of
the knee joint has been consistently reported to be an associated or risk factor for OSD [3–5]. Nonetheless, ROM is influenced
by contractile and non-contractile tissues and is therefore not a measure specific to muscle response. Hence, the relevance of
the mechanical properties of muscles in relation to OSD remains unclear.

⇑ Corresponding author at: Center for Liberal Arts, Meiji Gakuin University, 1518 Kamikurata-cho, Totsuka-ku, Yokohama 244-8539, Japan.
E-mail address: senomoto@gen.meijigakuin.ac.jp (S. Enomoto).

https://doi.org/10.1016/j.knee.2021.08.001
0968-0160/Ó 2021 Elsevier B.V. All rights reserved.
S. Enomoto, T. Oda, N. Sugisaki et al. The Knee 32 (2021) 140–147

Using ultrasound strain elastography, a recent study had shown that children with OSD had a harder patellar tendon and
that quadriceps muscle hardness was not significantly associated with the presence or absence of OSD [6]. Based on these
results, the mechanical properties of the quadriceps femoris muscle are not likely related to OSD.
Nevertheless, the aforementioned recent study had some issues concerning the measurement of muscle mechanical prop-
erties. First, Enomoto et al. [6] measured the resistance provided by the muscle against perpendicular pressure (i.e., muscle
hardness) [7]. However, the ROM of a joint is considered to be influenced by the longitudinal mechanical property of a mus-
cle (i.e., muscle stiffness).
Second, their experiment was conducted with the knee in the fully extended position only [6]. The relationship between
joint angle and muscle stiffness under passive conditions is non-linear [8,9]. Moreover, muscle stiffness affects joint stiffness
only in the joint position in which the muscle is sufficiently stretched [10]. Considering that children with OSD exhibit
reduced ROM (i.e., under the condition that the muscle is sufficiently stretched), the mechanical properties of the quadriceps
femoris muscle should be evaluated in joint positions in which the muscle is sufficiently stretched.
Third, muscle properties were evaluated in the resting condition only [6]. As OSD results from the repetitive strain on the
quadriceps femoris muscle [4], the mechanical properties of this muscle during contraction are thus assumed to be associ-
ated with OSD. Taking the absence of significant correlation between active and passive muscle stiffness into consideration
[11], evaluation of muscle stiffness under both resting and contracted conditions is necessary.
Shear-wave elastography is a technology that can localize muscle stiffness [12,13] and has recently been employed to
measure the stiffness of the quadriceps femoris muscle under stretched [9] and contracted [11] conditions. In our view,
the use of this technology can resolve the issue of measuring muscle hardness instead of muscle stiffness observed in the
study by Enomoto et al. [6]. We also considered that measuring muscle stiffness under stretched and contracted conditions
addresses the remaining two issues concerning the measurement of muscle mechanical properties, set out above. Addition-
ally, we hypothesize that compared with healthy children, children with OSD have a stiffer muscle during passive stretching
and contraction. Hence, the present study aimed to compare muscle stiffness during passive stretching and contraction
between children with and without OSD using shear-wave elastography in order to verify our hypothesis.

2. Materials and methods

The present study involved a total of 65 male junior high school basketball and volleyball players (130 legs). The biolog-
ical maturity of subjects was evaluated by years and months based on the peak height velocity (PHV) calculated from their
physical characteristics [14]. The age and physical characteristics of subjects who participated on the day of experiment (de-
scribed later in this paper) are presented in Table 1. This study was approved by the ethics committee of Hyogo University of
Teacher Education (approval no.: 2019–14). Prior to the survey, the purpose, content, method, and risks of this study were
explained to the children and their guardians, and written informed consent was subsequently obtained.

2.1. Study design and diagnosis of OSD

Measurements were performed on two separate days. On the day of diagnosis, orthopedic surgeons identified children
with OSD. On the day of the experiment, muscle stiffness was assessed using ultrasound shear-wave elastography. The inter-
val between the day of diagnosis and the day of the experiment was 1–4 weeks.
Diagnosis of OSD was based on the ultrasound diagnosis of OSD as reported in previous studies [15,16]. Orthopedic sur-
geons conducted assessments based on the presence of pain during exercise, protuberance, and tenderness over the tibial
tuberosity. OSD was defined as the presence of one or more of these factors along with the presence of free bone fragments
on the tibial tuberosity as well as cartilage swelling detected by ultrasonography. Free bone fragments were defined as
hyperechoic structures observed within the cartilage, which was hypoechoic aside from the secondary ossification. Cartilage
swelling was defined as an irregular surface on the skin due to the bulging cartilage. During ultrasound examination, the
subjects were seated with their knee joint flexed at 90°, and the probe was applied to the tibial tuberosity. The tibial tuberos-
ity was evaluated in the long-axis view using an ultrasound diagnostic imaging device (SonoSite M-Turbo; SonoSite Inc.,
Bothell, WA, USA) equipped with a HFL38/13-6 probe. A total of 21 subjects (28 legs; both legs in seven subjects and one
leg in 14 subjects) were identified as children with OSD, and a total of 44 subjects were identified as children without
OSD. We adjusted the schedule of the day of the experiment based on the results of the day of diagnosis. Because of time

Table 1
Age, years based on the peak height velocity (PHV), and physical charac-
teristics of the included subjects.

OSD group CON group

Age (years) 13.51 (0.81) 13.88 (0.88)
Height (cm) 161.97 (9.16) 162.40 (7.66)
Body weight (kg) 52.28 (10.51) 51.85 (7.52)
Years based on the PHV (years) 0.07 (0.97) 0.41 (0.78)

CON, control; OSD, Osgood–Schlatter disease.

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constraints regarding the schedule, we prioritized children with OSD to be measured on the day of the experiment. Healthy
children were measured as much as possible to obtain a sample size that was equal to the sample size of children with OSD.
Thus, all subjects that were diagnosed with OSD on the day of diagnosis (21 subjects) and 13 of the 44 subjects who were not
diagnosed with OSD, participated on the day of the experiment. Furthermore, on the day of the experiment, data for both legs
were obtained from children with OSD in both legs and from healthy children. For children with OSD in only one leg, data
were obtained for the affected side only. Finally, we allocated 28 legs with OSD and 26 legs without OSD to the OSD and the
control (CON) groups, respectively. The CON group did not include subjects with knee pain and a prior history of OSD
diagnosis.

2.2. Experiment 1. Muscle stiffness during passive stretching

The subjects were instructed to lie in the supine position on a table specifically designed to flex only the knee of the mea-
sured leg, with their entire body fully relaxed. The rectus femoris (RF) and vastus lateralis (VL) were examined. The RF and VL
stiffness was measured twice using shear-wave elastography for each of the following three conditions in random order: 0°
knee joint flexion (i.e., fully extended position), 45° knee joint flexion, and 90° knee joint flexion. Knee angles at 45° and 90°
knee joint flexion were monitored using an electronic goniometer (Biometrics Ltd., Newport, UK), which was placed on the
side of the knee joint and manually adjusted by the examiner (Fig. 1).
In this study, shear-wave velocity (SWV; in m/s) was used as an index of muscle stiffness. The SWV of muscles was mea-
sured using an ultrasound shear-wave elastography scanner (Aixplorer; Supersonic Imagine, Aix-en-Provence, France)
equipped with a linear array transducer (SL15-4) in the MSK preset. The location of the transducer (midpoint of the femur:
from the greater trochanter to the lateral epicondyle of the femur) was identified from B-mode ultrasonographic images and
was marked using a waterproof pen. The region of interest was manually set for each muscle. A typical example of SWV map
for each condition is presented in Fig. 1.

2.3. Experiment 2. Muscle stiffness during isometric contraction

The maximal voluntary isometric contraction (MVC) torque of the knee extensor was measured after Experiment 1. A
strain gauge (Takei Scientific Instruments Co., Ltd, Niigata, Japan) was attached between the steel frame and 3 cm above
the subjects’ lateral malleolus in order to register the MVC torque of the knee extensor. Knee and hip angles of 90° were used.
Finally, the joint torque was calculated by multiplying the force obtained by the strain gauge (N) and the moment arm of the
knee extensor mechanism (m) (from the center of rotation in the knee to 3 cm above the lateral malleolus). The force signal

Fig. 1. Typical elastogram of the rectus femoris (RF) and vastus lateralis (VL) obtained during passive knee flexion at 0°, 45°, and 90°.

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during MVCs was sampled at 1000 Hz using an analog-to-digital converter (PowerLab 16/35; ADInstruments, Sydney,
Australia).
After a standardized warm-up, MVCs were performed by subjects for 3 s and were repeated two or three times per sub-
ject. If the difference between two tests was greater than 10%, the subjects were required to perform a third test. The average
values of two tests were selected for analysis. If the subjects carried out a third test, the average values of the two closest
tests among the three tests were analyzed. After the MVC trial, the subjects performed an isometric knee extension exercise
for 7 s at 50% of MVC intensity. SWV was measured twice in random order for the two muscles. At least 1 min of rest was
provided between trials [17]. Measurement by ultrasound shear-wave elastography was the same as in Experiment 1. A typ-
ical shear-wave elastography image during contraction is shown in Fig. 2.

2.4. Data analysis

SWV analysis was conducted using the Q-Box software built into the ultrasound shear-wave elastography scanner. A Q-
box is a tool that quantifies the SWV of an area. In Experiment 1, the average value of three images was calculated for each
muscle and joint angle, and the average value of two measurements was utilized for analysis. In Experiment 2, taking the
mechanical delay of SWV mapping into account [18], five images (two to six within 7 s of contraction) were analyzed,
and the average value was considered to represent the condition. Furthermore, the average values of two trials were used
as representative values. In order to synchronize SWV and other data, the times on the computer and ultrasonic diagnostic
equipment were synchronized.

2.5. Statistical analysis

Average values and standard deviations of parameters were calculated. For the comparison between the OSD and CON
groups, height, body weight, age, and years based on the PHV were analyzed using the Welch’s t-test. Additionally, 95% con-
fidence intervals (CIs) for differences between mean values were shown, and the effect size (r) was calculated [19].
In this study, SWV and torque data for both legs were obtained from subjects who had OSD in both legs, as well as from
healthy children. These so-called ‘Nested designs’ yield data that cannot be considered to be independent; therefore, it vio-
lates the independency assumption of conventional statistical methods, such as the t-test or analysis of variance [20]. Hence,
we analyzed SWV and torque data using linear mixed models implemented in R statistical software version 4.0.5 [21]. As
mentioned above, because multiple observation of SWV and torque data were collected from one subject, we added the sub-
ject as a random effect to the models. In each analysis, we first ran models that included all fixed effects of interest along
with random effects (i.e., full models) and then simplified the models by removing non-significant terms (a > 0.05) from
the least-significant ones to arrive at a minimum adequate model using a backward stepwise deletion procedure [22]. Sta-
tistical significance of each fixed main effect and interaction was evaluated using likelihood ratio test comparing the change
in deviance between models. In multiple comparison, significant thresholds were adjusted using Bonferroni correction.
Some SWV data could not be analysed owing to ultrasonic diagnostic equipment malfunction. Therefore, in Experiment 1,
the sample size for the SWV of the RF was 27 in the OSD group and 25 in the CON group, whereas the sample size for the
SWV of the VL was 28 (no defect) in the OSD group and 25 in the CON group. In Experiment 2, the sample size for the SWV of
the RF was 26 in the OSD group and 26 (no defect) in the CON group. There was no defect in the VL in Experiment 2. The
intra-experimental reliability of each parameter was determined using two measurements. Coefficients of variation (CVs),
intraclass correlation coefficients (ICCs), and 95% CIs were also calculated.

Fig. 2. Typical elastogram of the rectus femoris (left) and vastus lateralis (right) obtained at 50% of maximal voluntary contraction.

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3. Results

The tested groups exhibited no significant difference with respect to age (P = 0.225, r = 0.25, 95% CI (-1.00, 0.25)), height
(P = 0.884, r = 0.03, 95% CI (-6.39, 5.54)), body weight (P = 0.892, r = 0.02, 95% CI (-5.90, 6.75)), and years based on the PHV
(P = 0.269, r = 0.20, 95% CI (-0.96, 0.28)).
The CV, ICC, and lower-bound and upper-bound 95% CIs are presented in Table 2. Except for the SWV of the VL at 0°, RF
during contraction, and VL during contraction, the ICCs ranged from 0.93 to 0.99 and were considered ‘almost perfect (0.81–
1.00)’. The ICCs for the SWV of the VL at 0°, RF during contraction, and VL during contraction were 0.80, 0.75, and 0.76,
respectively, and were considered ‘substantial (0.61–0.80)’ [23].
The SWV of the RF at each joint angle under resting conditions in the OSD and CON groups is shown in Fig. 3. The inter-
action between group and joint angle was significant (v2 = 7.114, df = 2, P = 0.029). The SWV was higher in the OSD group
than in the CON group at 45° (v2 = 4.522, df = 1, P = 0.033) and 90° (v2 = 4.440, df = 1, P = 0.035). No significant difference in
the SWV was observed between the two groups at 0° (v2 = 0.525, df = 1, P = 0.469).
The SWV of the VL at each joint angle under resting conditions in the OSD and CON groups is also shown in Fig. 3. Inter-
action between group and joint angle (v2 = 1.993, df = 2, P = 0.369) was not significant. Also, we found no significant main
effect of group (v2 = 0.013, df = 1, P = 0.908); however, the significant main effect of joint angle was observed (v2 = 282.8,
df = 2, P < 0.001). The SWV of the VL increased as the joint angle increased (0° vs. 45°: v2 = 39.01, df = 1, P < 0.001; 0° vs. 90°:
v2 = 192.8, df = 1, P < 0.001; 45° vs. 90°: v2 = 164.7, df = 1, P < 0.001).
No significant differences in the MVC torque (v2 = 0.344, df = 1, P = 0.558) and SWV of both muscles under contracted
conditions (RF: v2 = 0.394, df = 1, P = 0.530; VL: v2 = 0.064, df = 1, P = 0.800) were identified between the OSD group and
the CON group (Fig. 4). Additionally, there was no significant difference in the knee extensor torque at 50% of MVC between
the tested groups (during measurement for the SWV of the RF: v2 = 0.000, df = 1, P = 0.986; during measurement for the SWV
of the VL: v2 = 0.004, df = 1, P = 0.953).

4. Discussion

The present study compared muscle stiffness during passive stretching and contraction between children with and with-
out OSD and yielded the following main findings. First, children with OSD had a significantly stiffer RF during passive stretch-
ing than healthy children; nevertheless, such difference was not observed in the VL. Second, both RF and VL muscle stiffness
during contraction did not significantly differ between the two groups.
In the present study, RF stiffness was higher in the OSD group than in the CON group at knee joint flexion only (Fig. 3).
This finding suggests that a stiffer RF under stretched conditions is related to the presence of OSD, which supports our
hypothesis. No significant difference in VL stiffness was noted between the two groups at any knee angle. Using shear-
wave elastography, Xu et al. [9] investigated the relationship between knee joint angle and the passive stiffness of the RF,
VL, or vastus medialis oblique (VMO). They observed significant differences between the RF and VL or VMO at knee flexion
angles over 54° and reported that RF stiffness increased more sharply at knee flexion than VL and VMO stiffness. These
results imply that knee flexion ROM is strongly influenced by RF stiffness. Considering previous evidence and our observa-
tions, we believe that increased RF stiffness was reflected in the reduced knee flexion ROM observed in children with OSD [3–
5,24].
OSD is a disease in which partial detachment or inflammation occurs as a consequence of repeated traction on the tibial
tuberosity during growth [25]. In other words, the degree of stress applied to the tibial tuberosity is assumed to be associated

Table 2
Intra-experimental reliability of measured parameters.

CV (%) 95% CI lb 95% CI ub ICC 95% CI lb 95% CI ub

SWV
RF Passive 0° 2.37 1.71 3.03 0.93 0.87 0.96
Passive 45° 3.02 2.36 3.68 0.94 0.90 0.97
Passive 90° 1.97 1.56 2.37 0.99 0.98 0.99
50% MVC 5.35 4.07 6.64 0.75 0.57 0.86
VL Passive 0° 3.37 2.45 4.28 0.80 0.65 0.88
Passive 45° 2.26 1.77 2.76 0.93 0.88 0.96
Passive 90° 1.95 1.46 2.44 0.95 0.91 0.97
50% MVC 4.66 3.56 5.76 0.76 0.59 0.86
Torque
MVC 2.37 1.95 2.78 0.98 0.97 0.99
50% MVC-RF 1.55 1.16 1.94 0.99 0.99 1.00
50% MVC-VL 1.42 1.04 1.79 0.99 0.99 1.00

CI, confidence interval; CV, coefficient of variation; lb, lower bound; MVC, maximal voluntary contraction; RF, rectus femoris; SWV, shear-wave velocity; ub,
upper bound;
VL, vastus lateralis.

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Fig. 3. Shear-wave velocity of the rectus femoris (RF) and vastus lateralis (VL) during passive stretching in the tested groups. *P < 0.05. The main effect of
joint angle was significant in VL (P < 0.001). CON, control; N.S., not significant; OSD, Osgood–Schlatter disease.

Fig. 4. Shear-wave velocity of the rectus femoris (RF) and vastus lateralis (VL) at 50% of maximal voluntary contraction in the two groups. CON, control; N.
S., not significant; OSD, Osgood–Schlatter disease.

with OSD. In the present study, the OSD group had a significantly stiffer RF under stretched conditions only. Muscle stiffness
is influenced by muscle fiber composition, with type I muscle fibers being stiffer than type II muscle fibers under passive
conditions [26]. Because fat is more compliant than muscles [27], intramuscular fat can also affect muscle stiffness, as mea-
sured by ultrasound shear-wave elastography. Furthermore, it has been suggested that noncontractile connective tissues
(e.g., endomysium, perimysium, epimysium) can affect passive muscle stiffness [28]. Given that a significant difference in
the SWV of the RF was observed between the groups under stretched conditions only, it is unlikely that these factors were
responsible for such a difference. In contrast, the difference in slack length, which affects the SWV of the muscle when it is
stretched, may have contributed to the present results. Slack length is a crucial parameter used in muscle models and influ-
ences the characteristics of muscles, including the force–length relationship [29]. Albeit speculative, the slack length of the
RF might be related to the presence of OSD by increasing the muscle force due to changes in muscle characteristics, including
the force–length relationship. Unfortunately, to our knowledge, no objective evidence exists that supports this view. Consid-
ering the absence of a significant difference in the SWV of the VL between the tested groups, elucidating the effects of each
muscle’s properties on the degree of stress applied to the tibial tuberosity could clarify the relationship between muscle
properties and OSD.
Several previous studies have reported that children with OSD exhibit reduced knee flexion ROM [3–5,24]. However, this
type of measure does not provide any information about the muscle or tendon [30] because musculotendinous structures
can affect joint flexibility [31–33]. In the present study, we expanded these observations by directly measuring muscle stiff-
ness in children with OSD.

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Static stretching is integral to OSD prevention and early recovery [34,35]. A previous study investigated the effects of sta-
tic stretching training on muscle stiffness using elastography and showed that static stretching training could indeed reduce
muscle stiffness [36]. Hence, muscle stiffness reduction via stretching training may be useful in preventing OSD and achiev-
ing early recovery. Flexing the knee joint to stretch the quadriceps [34] and stretching the RF with hip extension have been
suggested for children with OSD [34,35]. Our results suggest that stretching the RF is more effective. In addition to knee flex-
ion, stretching in the extended hip position might be effective in preventing OSD and improving symptoms by reducing RF
stiffness.
As mentioned above, the degree of stress applied to the tibial tuberosity is a key factor in OSD, and muscle strength, mus-
cle stiffness, and muscle activity during movement (e.g., pre-activation) affect the stress applied to the tibial tuberosity. In
this study, the SWV of the RF and VL during contraction showed no significant difference between the tested groups (Fig. 4),
indicating that muscle stiffness during contraction has a limited effect on OSD, which is not consistent with our hypothesis.
Similarly, MVC did not significantly differ between the groups. We examined active muscle stiffness and muscle strength
during isometric contraction in our study, and the lack of statistical difference in active muscle stiffness and muscle strength
between the groups might be related to the type of muscle contraction used in our study.
Because OSD is a common condition primarily among boys engaged in sporting activities that require jumping (e.g., soc-
cer, running, basketball, volleyball, gymnastics) [37], the mechanical properties or behaviors of the muscle during the afore-
mentioned sporting activities are thus speculated to be related to OSD. Furthermore, the change in muscle activity could be
related to OSD by increasing the rate of increase in the contractile force (i.e., rate of force development) during ballistic
movement. Further studies are required to clarify the biomechanical characteristics of children with OSD during a movement
task.
The present study has certain limitations. First, we could not evaluate the slack length of muscles, as we measured the
SWV at three knee joint angles only. Second, we could not mention the risk factors for OSD owing to the cross-sectional
design of our study. Further longitudinal studies are warranted to confirm whether the mechanical characteristics of the
quadriceps muscle are indeed associated with OSD onset.

5. Conclusions

The present study compared the SWV of the RF and VL during passive stretching and contraction between children with
OSD and healthy children and showed that children with OSD had higher SWV of the RF under stretched conditions. No sig-
nificant differences in both muscles under unstretched conditions, in the VL under stretched conditions, and in the SWV of
both muscles under contracted conditions were observed between the tested groups. These results suggest that a stiffer RF
under stretched conditions is related to the presence of OSD and that both muscles under unstretched and contracted con-
ditions and the VL under stretched conditions have limited association with the presence of OSD. The study results have
important implications for the understanding the association between the mechanical properties of muscles and OSD.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper.

Acknowledgments

The authors acknowledge the help of Aiko Tsushima, Ayano Wada, Haruna Yokoyama, Kenta Yoshimura, Kota Miyake,
Masakazu Matsueda, Nana Kojima, Nao Naya, Ryota Tanaka, Ryotaro Konya, Satsuki Uemura, Shungo Nakayama, Takashi
Hoshishima, Takeshi Omori, Yuta Ishii, and Yuya Kobashi in the experiments. The authors thank them and all subjects
who participated in this study. We would like to thank Editage (www.editage.jp) for English language editing.

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