Pathogenic Factors Associated With Osgood-Schlatter Disease in Adolescent Male Soccer Players
Pathogenic Factors Associated With Osgood-Schlatter Disease in Adolescent Male Soccer Players
Pathogenic Factors Associated With Osgood-Schlatter Disease in Adolescent Male Soccer Players
Background: A previous cross-sectional study reported that pathogenic factors associated with Osgood-Schlatter disease (OSD)
in adolescent athletes include increased quadriceps muscle tightness, lower leg malalignment, and development of apophysitis in
the tibial tuberosity.
Purpose: To confirm these pathogenic factors associated with OSD in a longitudinal study with regard to physical function and
performance.
Study Design: Cohort study; Level of evidence, 2.
Methods: In this study, 37 boys (mean age, 10.2 ± 0.4 years) were recruited from 2 soccer teams at an elementary school. This
cohort study was conducted over an observation period of 1 year, with measurements recorded at baseline, followed by screening
for OSD every 6 months. Variables evaluated at baseline included physical function (morphometry, joint flexibility, and lower
extremity alignment), presence of Sever disease, and kicking motion.
Results: Pathogenic factors associated with OSD in the support leg of adolescent male soccer players included height, weight,
body mass index, quadriceps femoris muscle tightness in the kicking and support legs, and gastrocnemius muscle tightness,
soleus muscle tightness, and medial longitudinal arch in the support leg. Additional factors included a diagnosis of Sever disease
and distance from the lateral malleolus of the support leg’s fibula to the center of gravity during kicking.
Conclusion: The onset of OSD was found to be affected by many factors, including developmental stage, physical attributes, and
pre-existing apophysitis. In particular, a diagnosis of Sever disease and backward shifting of the center of gravity during kicking
increased the risk of the subsequent onset of OSD, suggesting that these factors are very important as a possible focus for
interventions.
Keywords: knee; pediatric; growth; ultrasonography; prevention
Soccer is a sport that is currently enjoyed worldwide and example, elbow joint injuries in baseball players and knee
can be played from childhood into adulthood. As such, soc- joint injuries in soccer players.19
cer is effective in increasing the activity of both children Osgood-Schlatter disease (OSD), named for the physi-
and elderly people. However, adolescent soccer players cians who first described it in 1903, is a type of osteochon-
exhibit many musculoskeletal disorders resulting from drosis. OSD is traction apophysitis resulting from the
repeated biomechanical stress.27 Children who are active repeated contraction of the quadriceps femoris muscle on
during a growth spurt may develop multiple sites of epiphy- the tibial tuberosity.13,22 The onset of OSD is related to
sitis, and many sport injuries in adolescent athletes are activities and performance specific to sports such as soc-
caused by the architectural fragility of the epiphysis, for cer, basketball, and volleyball. 31 In particular, OSD
accounts for the highest incidence of knee joint injuries
in adolescent male soccer players.24,30 To date, pathogenic
The Orthopaedic Journal of Sports Medicine, 6(8), 2325967118792192
factors reportedly associated with OSD in adolescent ath-
DOI: 10.1177/2325967118792192 letes include increased quadriceps muscle tightness, lower
ª The Author(s) 2018 leg malalignment, and development of apophysitis in the
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1
2 Watanabe et al The Orthopaedic Journal of Sports Medicine
*Address correspondence to Hiroyuki Watanabe, PhD, PT, Department of Rehabilitation, School of Allied Health Sciences, Kitasato University, 1-15-1
Kitasato, Sagamihara, Kanagawa 252-0373, Japan (email: hw@ahs.kitasato-u.ac.jp).
†
Department of Rehabilitation, School of Allied Health Sciences, Kitasato University, Sagamihara, Japan.
‡
Nishifuna Clinic, Funabashi Orthopedic Hospital, Funabashi, Japan.
§
Department of Physical Therapy, Faculty of Health and Medical Science, Teikyo Heisei University, Tokyo, Japan.
||
Department of Rehabilitation, Kitasato Institute Hospital, Kitasato University, Tokyo, Japan.
{
Department of Orthopedic Surgery, School of Medicine, Kitasato University, Sagamihara, Japan.
The authors declared that they have no conflicts of interest in the authorship and publication of this contribution.
Ethical approval for this study was obtained from the Kitasato University School of Allied Health Sciences Ethics Committee (2011-2018).
The Orthopaedic Journal of Sports Medicine Pathogenic Factors of Osgood-Schlatter Disease 3
TABLE 1
ICCs From Muscle Tightness Testsa
tibia after the knee joint was maximally extended was mea-
sured as hamstring muscle tightness.
Figure 2. Positioning for measuring muscle tightness: (A) Gastrocnemius Muscle Tightness. To measure gastroc-
iliopsoas, (B) quadriceps, (C) hamstring, (D) gastrocnemius, nemius muscle tightness, the ankle joint dorsiflexion angle
and (E) soleus muscles. was measured when maximally dorsiflexed in the supine
position, with the knee extended and maintained in a neu-
We used general joint laxity tests in this study. The 7 con- tral position relative to the varus-valgus angle of the ankle.
ditions measured included thumb to forearm position, elbow Soleus Muscle Tightness. To measure soleus muscle
hyperextension of 15 , shoulder hyperrotation, hip hyper– tightness, the ankle joint dorsiflexion angle was measured
external rotation of 90 in the standing position, knee when maximally dorsiflexed in the prone position with the
hyperextension of 10 , ankle hyperdorsiflexion of 45 in knee at 90 of flexion.
knee flexion, and anteflexion of the trunk. Positive shoulder
hyperrotation was defined as when participants could clasp Lower Leg Alignment
their hands from both the cranial and caudal sections of their
back. Positive hip hyper–external rotation was defined as The Q-angle was measured with the participants in a
when participants could maintain their hips at 90 of external supine position. A protractor, remodeled for Q-angle mea-
rotation with both their lower legs in a neutral position. Pos- surement, was centered over the patella, with one limb over
itive forward flexion of the trunk was defined as when parti- the tibial tubercle and the other in line with the anterior
cipants could touch the floor with the bilateral palms of their superior iliac spine.
hands while maintaining their lower legs in an extended posi- For medial longitudinal arch (MLA) measurement, par-
tion. For each condition, 1 point was given when range of ticipants were asked to assume a relaxed standing position
motion reached or exceeded baseline. The wrist, elbow, shoul- on both legs, looking straight ahead with their arms by
der, knee, and ankle received half a point for each side. Total their sides. The MLA was measured as the ratio of the
scores were calculated, with a maximum total score of 7. length from the posterior heel to the first metatarsophalan-
geal joint and the height from the floor to the navicular
tubercle.28,29
Muscle Tightness Testing
Muscle tightness tests were performed on the iliopsoas, Diagnosis of OSD and Sever Disease
quadriceps femoris, hamstring, gastrocnemius, and soleus
muscles on both sides (Figure 2).32 All measurements of Examinations were conducted using M-Turbo (SonoSite)
muscle tightness were repeated twice by a single skilled and 13-MHz (6-13 MHz) linear probes (Figure 3). To meas-
physical therapist (H.W.) who demonstrated excellent ure the skeletal maturation of the distal attachment of the
intrarater reliability on all muscle tightness measures patellar tendon, participants were placed in a supine posi-
(Table 1). tion with the knees bent. Ultrasound was performed in the
Iliopsoas Muscle Tightness. The iliopsoas muscle mea- long axis view, focusing on the patellar tendon attach-
surement was performed by obtaining the angle of the hip ment.36 The bone growth stage of the tibial tuberosity on
joint when passively bending the opposite hip joint to the ultrasound was defined using the Ehrenborg classification
maximum in a supine position (Thomas test position). as cartilaginous, apophyseal, epiphyseal, or bony.9
Quadriceps Muscle Tightness. The quadriceps muscle All research in this study was conducted on the soccer
measurement was performed by bending the angle of the grounds or practice field; none was carried out at medical
knee joint in a prone position. Muscle tightness was estab- institutions. For this reason, it was impossible to use diag-
lished in the quadriceps femoris muscle if the participant’s nostic imaging (eg, radiography, computed tomography,
buttocks were lifted by muscle tension during the magnetic resonance imaging). Ultrasonography was also
measurement. used to detect pathological features and monitor the course
Hamstring Muscle Tightness. Hamstring muscle tight- of OSD. A diagnosis was made based on tenderness of the
ness was established from the measurement position of 90 tibial tuberosity, the presence or extent of irregular results
in the hip and knee joint in a supine position. The angle on imaging, and thickened cartilage of the tibial tuberosity
between the vertical line to the floor and the long axis of the visible on ultrasound.6
4 Watanabe et al The Orthopaedic Journal of Sports Medicine
Figure 3. Linear probe positioning on the patellar tendon attachment and Achilles tendon attachment as well as examples of typical
ultrasound images taken in the longitudinal axis to diagnose (A) Osgood-Schlatter disease and (B) Sever disease.
Biomechanical Analysis
Reflective markers with a diameter of 1 cm were fixed in
25 places across the body: top of the head, earlobe (occip-
ital), and superior border of the sternum; both acromia,
elbow joints, wrist joints, third metacarpophalangeal
joints, greater trochanters, knee joints, lateral malleoli,
toes, heels, and iliac crests; and on the spinous processes
of the eighth thoracic vertebra and the superior border of
the sacrum (Figure 4). The 3D coordinates of the markers
were calculated using a 3D video motion analysis system
(Frame-DIAS IV; DKH). Participants wore the black
spats and footwear typically used in practice and competi-
tions. Measurements of the COG were obtained according
to the method provided by Yokoi et al37 using body part
coefficients. A net was assembled 3 m away from the ball
and 1 m above the ground to measure kicking action (Fig-
ure 5). Four high-speed cameras (EXILIM EX-F1; Casio)
were arranged at intervals of 4.5 m at 60 , 150 , 210 , and
330 around the participant. Filming continued until the
ball hit the target 3 times.
Of the 3 filmed trials, the trial with the greatest ball
impact was used for analysis. Kicking measurements were
made based on the distance of the lateral malleolus of the Figure 4. Reflective marker placement on the body.
support leg’s fibula from the COG during the kicking phase level of significance was set to 5%, and a 2-tailed test (Stu-
(COG distance). The COG distance at foot contact and at dent t test) was performed. After selecting the presence of
ball impact were also calculated (Figure 6). OSD as the dependent variable, the odds ratio (OR) and
95% CI for each item were calculated using univariate anal-
Statistical Analysis ysis. The coefficient of determination (Nagelkerke R2) and
effect size (f 2) for logistic regression analysis were also
The data were analyzed with SPSS v 22.0 (IBM). Means calculated. When f 2 > 0.35, it represented a large effect;
and SDs were calculated from the baseline data and com- 0.35 f 2 > 0.02 represented a medium effect; and
pared between the OSD group and non-OSD group. The f 2 0.02 represented a small effect.5
The Orthopaedic Journal of Sports Medicine Pathogenic Factors of Osgood-Schlatter Disease 5
RESULTS
Table 2 shows the results of the physical examination and
3D biomechanical analysis for the 36 study participants.
OSD was found in the support leg of 12 participants (inci-
dence rate: 33.3%) but was not found in the kicking leg of
any participant during the observation period. At baseline,
13 participants were diagnosed with Sever disease (preva-
lence rate: 36.1%). We identified 48 knees in the cartilagi-
nous stage, 16 knees in the apophyseal stage, and 8 knees
in the epiphyseal stage according to the Ehrenborg 9
classification.
Of the variables investigated, height (OR, 1.31 [95% CI,
1.06-1.63]; P ¼ .015), weight (OR, 1.37 [95% CI, 1.10-1.71];
P ¼ .005), BMI (OR, 1.92 [95% CI, 1.18-3.12]; P ¼ .009),
quadriceps femoris muscle tightness in the kicking leg
(OR, 0.84 [95% CI, 0.74-0.96]; P ¼ .009), quadriceps femoris
muscle tightness in the support leg (OR, 0.87 [95% CI, 0.78-
0.97]; P ¼ .015), gastrocnemius muscle tightness in the
Figure 5. Typical view of kicking recordings. A net was set up support leg (OR, 0.85 [95% CI, 0.74-0.98]; P ¼ .026), soleus
3 m away from the ball with a target 1 m above the ground. muscle tightness in the support leg (OR, 0.89 [95%
Figure 6. Center of gravity (COG) distance was measured as the distance from the lateral malleolus of the support leg’s fibula to the
COG during the kicking phase: (A) foot contact and (B) ball impact.
TABLE 2
Results of Physical Examination and 3-Dimensional Biomechanical Analysis at Baselinea
MTT, deg
Iliopsoas 5.0 ± 3.7 4.2 ± 4.2 4.4 ± 3.3 3.8 ± 3.9
Quadriceps 37.5 ± 7.5 36.3 ± 7.7 45.0 ± 6.0 44.0 ± 7.1
Hamstring 42.5 ± 9.2 45.8 ± 11.2 39.8 ± 6.5 41.0 ± 7.9
Gastrocnemius 7.1 ± 5.4 7.9 ± 5.0 11.2 ± 6.7 12.8 ± 6.3
Soleus 21.3 ± 6.8 21.3 ± 6.8 27.8 ± 8.5 27.6 ± 8.8
Lower leg alignment
Q-angle, deg 12.8 ± 2.9 12.5 ± 2.6 12.1 ± 3.0 11.0 ± 3.4
MLA, % 22.0 ± 2.4 21.1 ± 2.2 20.3 ± 3.5 19.1 ± 3.2
COG distance, cm
Foot contact 74.5 ± 5.0 79.3 ± 2.8
Ball impact 64.8 ± 4.4 67.1 ± 3.6
a
Values are reported as mean ± SD. BMI, body mass index; COG, center of gravity; GJL, general joint laxity; MLA, medial longitudinal
arch; MTT, muscle tightness test; OSD, Osgood-Schlatter disease.
6 Watanabe et al The Orthopaedic Journal of Sports Medicine
TABLE 3
Findings of Univariate Analysis for Explored Intrinsic Factorsa
CI, 0.79-0.99]; P ¼ .033), MLA of the support leg (OR, 1.35 support leg muscles (quadriceps femoris, gastrocnemius,
[95% CI, 1.02-1.80]; P ¼ .039), Sever disease diagnosis and soleus), MLA in the support leg, diagnosis of Sever
(OR, 5.25 [95% CI, 1.28-21.57]; P ¼ .021), and COG distance disease, and location of the COG shifting backward during
at foot contact (OR, 1.41 [95% CI, 1.07-1.87]; P ¼ .016) kicking.
were identified as pathogenic factors associated with OSD With regard to muscle tightness, previous studies have
(Table 3). The 12 participants diagnosed with OSD received demonstrated that greater tightness in the quadriceps
immediate medical follow-up. femoris, biceps femoris, gastrocnemius, and soleus muscles
is associated with the development of OSD.23,34 Because
adolescence is a developmental stage, growth along the lon-
DISCUSSION gitudinal axis of the body is extensive. 26 This growth
enhances muscle tightness and results in characteristically
In this study, the incidence rate of OSD was 33.3%. Previ- reduced muscle flexibility during adolescence. Certain fea-
ous studies on adolescents have reported OSD incidence tures of adolescent soccer players may further reduce mus-
rates ranging from 9.8% to 21%.7,20,23 There are 2 possible cle flexibility, increasing OSD susceptibility. In particular,
reasons why the incidence of OSD was higher in this study.
reduction of muscle tightness in the quadriceps increases
First, the longitudinal investigation of 10-year-old boys in
traction stress on the secondary ossification center of the
this study resulted in a higher percentage than the onset
tibial tuberosity.
rate found in adolescents in previous studies (maximum
Although the present findings indicate that the onset of
age range, 15-18 years). OSD is known to occur as a result
OSD is more likely to occur when the MLA is higher, a
of traction stress on the secondary ossification center of the
formative MLA is advantageous because it functions as a
tibial tuberosity by the patellar tendon. For this reason, the
shock absorber. The foot arch developed to enable bipedal
onset of OSD is strongly related to the growth process of
walking. The foot also changes with development, and suf-
the secondary ossification center of the tibial tuberosity.4
This growth process is classified into 4 stages: the cartilag- ficient foot development is necessary to ensure the shock-
inous stage (ages 0-11 years), the apophyseal stage (ages absorbing function. Because foot development peaks at
11-14 years), the epiphyseal stage (ages 14-18 years), and approximately 10 years old, the participants in this study
the bony stage (ages >18 years).8 It has been reported that were considered to have already reached peak develop-
the onset of OSD occurs more frequently in the apophyseal ment.15,33 The MLA may be associated with other develop-
stage of development.4 The mean age of the participants in mental factors such as height, weight, and BMI, which also
this study (10.2 ± 0.4 years) is close to the apophyseal stage. affect OSD onset. Thus, the MLA results in this study were
It seems that the peak age for the onset of OSD may occur interpreted to be a confounding factor rather than evidence
at younger than 15 to 18 years. The second possible reason of the influence of foot architecture.
is that in this study, the morphology of the tibial tuberosity The age of onset of Sever disease is from 8 to 10 years in
was assessed using ultrasonography. Ultrasonography is boys, which is younger than the age of onset of OSD.25 In
superior at observing the cartilage under the quadriceps the present study, a diagnosis of Sever disease had an OR of
femoris muscle attachment; thus, the diagnostic accuracy 5.25, which was very high compared with the other factors
of OSD in this study may be greater than that of previous identified. It has been reported that the incidence rate of
studies.4,11 Sever disease is higher in players of high-impact sports or
Based on the baseline data, pathogenic factors associated sports with high activity levels.1 Because the onset of OSD
with OSD in the support leg were identified as height, is also influenced by the level of activity, it appears that
weight, BMI, increased muscle tightness in the quadriceps OSD occurs after the onset of Sever disease. As the pres-
femoris of the kicking leg, increased muscle tightness of the ence of Sever disease makes the onset of OSD 5 times more
The Orthopaedic Journal of Sports Medicine Pathogenic Factors of Osgood-Schlatter Disease 7
likely, we consider that interventions are necessary for including the stage of development, physical function, the
those who have Sever disease to prevent the onset of OSD. onset of preceding apophysitis, and a backward-positioned
A characteristic of the kicking motion used in soccer is COG while kicking. To prevent OSD, it is necessary to
that the trunk is in an upright position when the soccer address each factor that may be related to its onset. In
player makes impact with the ball.10 However, when soccer particular, a diagnosis of Sever disease and a posterior
players intend to perform a strong kick, postures in which COG during kicking increased the risk of OSD, suggesting
the trunk is inclined backward are observed with high fre- that these may be important factors to consider when tak-
quency. A study by Blackburn and Padua3 reported that ing preventative measures.
quadriceps muscle activity decreased as the COG position
approached the knee joint after landing. It has been sug-
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