obesity cuadriceps
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Eur J Appl Physiol (2008) 103:481–484
DOI 10.1007/s00421-008-0737-3
123
SHORT COMMUNICATION
Quadriceps muscle function characteristics in severely
obese and nonobese adolescents
Nicola A. MaYuletti · Marc Jubeau · Fiorenza Agosti ·
Alessandra De Col · Alessandro Sartorio
Accepted: 24 March 2008 / Published online: 4 April 2008
© Springer-Verlag 2008
Abstract The purpose of this cross-sectional study was to
compare quadriceps muscle strength and fatigue between
severely obese (body mass index 34 kg/m2) and nonobese
adolescents. Maximal isokinetic torque and angle of peak
torque as well as isometric torque at short (40° of knee Xex-
ion) and long (80° of knee Xexion) muscle length were
measured using an isokinetic dynamometer. Muscle fatigue
was quantiWed as the percent torque loss during an isoki-
netic voluntary protocol and an electrical stimulation iso-
metric protocol. Obese adolescents produced greater
absolute isokinetic (+16%; P < 0.05) and isometric torque
at short (+25%; P < 0.01) but not at long muscle length
(P > 0.05) compared to their lean counterparts. The angle
of peak torque was signiWcantly lower in obese than in non-
obese subjects (¡11%; P < 0.05), i.e., obese produced their
maximal strength at shorter muscle length. Isokinetic and
isometric torque normalized to the fat-free mass were not
signiWcantly diV erent between the two groups. No signiW-
cant diV erence in voluntary and stimulated torque loss was
observed between groups. Muscle strength per unit of fat-
free mass and muscle fatigue were similar in the obese and
nonobese adolescents tested in this study, therefore
suggesting that obesity has little or no eV ect on quadriceps
muscle function characteristics. On the other hand, it
remains to be conWrmed whether the observed quadriceps
muscle length speciWcity contributes to the reduced func-
tional capacity of obese adolescents during complex motor
tasks involving deep knee Xexion (squatting, kneeling).
Keywords Peak torque · Fatigue · Muscle length ·
Isometric · Isokinetic
Introduction
Although it is generally admitted that young obese sub-
jects—who are ridiculed because of body size and form and
who are more likely to voluntarily reduce habitual physical
activity (Parizkova and Hills 2001)—would exhibit inade-
quacies in the performance of motor tasks (Beunen et al.
1983; Korsten-Reck et al. 2007), very few studies have
attempted to compare motor performance between obese
and nonobese adolescents. SpeciWcally, the function of the
quadriceps femoris muscle—which is responsible for knee
extensor torque production and therefore plays a key role
during ambulatory, functional and sport activities—has
been investigated only in one instance. Blimkie et al.
(1990) measured maximal voluntary isometric and isoki-
netic strength of the quadriceps muscle in obese (mean
body mass index 31 kg/m2) and nonobese male adolescents
(mean age 16.6 years). They reported no signiWcant diV er-
ences between groups for absolute strength, fat-free body
mass, lean thigh area, and contractile properties, therefore
suggesting that muscular factors do not contribute to the
poorer motor performance of the young obese. It would be
interesting to know if the quadriceps muscle of severely
obese adolescents, who present greater fat-free mass (in
addition to fat mass) than their lean pairs (Lazzer et al.
N. A. MaYuletti (&)Neuromuscular Research Laboratory, Schulthess Klinik,
Lengghalde 2, 8008 Zurich, Switzerland
e-mail: [email protected]
M. Jubeau
Laboratoire INSERM U887, Faculté des Sciences du Sport,
Université de Bourgogne, Dijon, France
F. Agosti · A. De Col · A. Sartorio
Laboratorio Sperimentale di Ricerche Endocrinologiche,
Istituto Auxologico Italiano, IRCCS,
Piancavallo (VB) e, Milan, Italy
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482 Eur J Appl Physiol (2008) 103:481–484
123
2007), would produce greater absolute strength, similar to
adults who are severely obese (MaYuletti et al. 2007).
To our knowledge, the eV ect of obesity on muscle
fatigue, which—besides muscle strength—represents an
important link to normal daily-living tasks, has never been
addressed in adolescents. This information is essential since
several daily (e.g., stair climbing, walking) as well as sport
activities (e.g., cycling, running) involve repetitive contrac-tions of the quadriceps muscles, where possible greater
fatigue in the obese (MaYuletti et al. 2007) could be seen
as a limiting factor for motor performance.
The main objective of this study was to compare quadri-
ceps muscle strength and fatigue characteristics between
severely obese and nonobese adolescents, in an attempt to
determine if factors other than fatness may account for poor
motor performance capacity in obesity.
Methods
Subjects
Ten severely obese (body mass index >97th percentile)
male adolescents (age ¸13 and ·17 years) volunteered to
participate in this study (mean age § SD 15.6 § 1.2 years;
height 171 § 6 cm; body mass index 34 § 3 kg/m2). Ten
age- and height-matched (age 14.9 § 1.1 years; height
170 § 9 cm; body mass index 19§ 1 kg/m2) nonobese
male adolescents recruited from the hospital staV families
were also tested. Maturity level (estimated according to
Tanner staging) was comparable between groups (15% of
Tanner stage III, 50% of stage IV and 35% of stage V).
Physical activity level was also similar between groups; all
the adolescents performed recreational physical activity for
¸2 h/week within the past month and none of them was
involved in very vigorous physical activity. None of the
adolescents had orthopedic or cardiovascular problems
interfering with the execution of the tests. Signed informed
parental permission and signed informed assent of each
individual were obtained. The study protocol was approved
by the Ethics Committee of the Italian Institute for Auxol-
ogy. All the procedures were conducted according to
Helsinki Declaration.
Fat-free mass estimation
Bioelectric impedance analysis was performed in the early
morning after an overnight fast, according to a conventional
standard technique (Lukaski et al. 1986). Subjects were
asked not to drink within 4 h of the test, to empty their uri-
nary bladder at least 30 min before the analysis, and to
remain in the supine position for 5 min before the acquisi-
tion. The electrodes were placed on the right wrist and ankle
of the subjects while lying comfortably supine in a bed with
the limbs abducted from the body. Whole-body resistance to
an applied current (at 1, 5, 10, 50 and 100 kHz, 0.8 mA) was
measured with a tetrapolar device (Human IM, Dietosystem,
Milan, Italy). Fat-free mass was calculated with the speciWc
equations derived by Gray et al. (1989).
Isokinetic and isometric muscle function
Details of the testing procedures have been reported previ-
ously (MaYuletti et al. 2007). In brief, assessments con-
sisted of isokinetic and isometric quadriceps muscle
strength and fatigue over two testing sessions (session 1:
isokinetic; session 2: isometric; interval: 24 h). The right
quadriceps muscle was tested by using an isokinetic dyna-
mometer (Cybex, Lumex, Ronkonkoma, NY, USA). Sub-
jects were comfortably seated (90° at the hip) on the
dynamometer chair. The dynamometer lever arm was
attached 2–3 cm above the lateral malleoulus by using a
strap. Straps were also applied across the chest, pelvis and
mid-thigh. Torque data were corrected for gravity using
Cybex software. Visual feedback and verbal encourage-
ment from the investigator were consistently provided.
Warm-up consisted of several submaximal contractions of
the quadriceps muscle at diV erent angular velocities and
knee joint positions.
Muscle strength
Isokinetic measurements involved 3–4 consecutive (maxi-
mal) knee extensions performed at an angular velocity of
180°/s. Range of motion was 90°, from 90° of Xexion to 0°
(knee fully extended). All knee angles were provided by the
isokinetic device. We consistently assumed that knee joint
angle was linearly related to quadriceps muscle length (0° of
Xexion: shortest quadriceps length; 90° of Xexion: longest
quadriceps length). Isometric measurements consisted of
two maximal knee extensions realized at two diV erent joint
positions (randomly presented): 40° of knee Xexion (short
quadriceps muscle length) and 80° of knee Xexion (long
quadriceps muscle length). Rest periods of »2 min were
allowed between series of contractions. For isokinetic trials,
peak torque and angle of peak torque were measured. For
isometric trials, the maximal torque at the two knee joint
positions was retained. In each case, only the best perfor-
mance was included in the analyses. Both isokinetic and iso-
metric torque data were recorded as absolute values (Nm)
and subsequently normalized to fat-free mass (Nm/kg).
Muscle fatigue
The voluntary isokinetic fatigue test consisted of 50 con-
secutive knee extensions completed at an angular velocity
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Eur J Appl Physiol (2008) 103:481–484 483
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of 180°/s. The average peak torque of the Wrst three con-
tractions was considered as the reference value (100%).
Voluntary fatigue was then expressed as the percent torque
loss with respect to the reference after 10, 20, 30, 40 and 50
contractions (average of 3–5 peak torque values).
The stimulated fatigue test was completed under isomet-
ric conditions (60° at the knee) and consisted of 60 trains of
stimuli (1.5 s on ¡3.5 s oV ; frequency 40 Hz; pulse dura-tion 600 s) delivered over a 5-min period. A commercially
available stimulator was used (Compex Sport-P, Medicom-
pex SA, Ecublens, Switzerland). Stimulating electrodes
were placed over the vastus lateralis and vastus medialis
motor points (25 cm2 each), and proximal to the femoral tri-
angle (50 cm2). Current amplitude was progressively
increased to attain 10% of the maximal voluntary isometric
torque. The average torque of the Wrst three contractions
was considered as the reference value (100%). Stimulated
fatigue was then expressed as the percent torque loss with
respect to the reference after 1, 2, 3, 4 and 5 min (average
of 3–5 peak torque values).
Statistical analyses
Statistical methods including means and their SD or SE
were calculated for each parameter. Statistical diV erences
between obese and nonobese adolescents were assessed
using unpaired (one-tailed) t tests. The level of signiWcance
was established at P < 0.05.
Results
Muscle strength
Absolute isokinetic torque was signiWcantly higher in obese
than in nonobese adolescents (+16.3%; P < 0.05), while
isokinetic torque normalized to the fat-free mass was almost
identical between the two groups (Table 1). The angle of
peak torque was signiWcantly smaller in obese than in non-
obese subjects (»6°; P < 0.05), that is to say obese adoles-
cents produced their maximal strength at shorter quadriceps
muscle length compared to their lean counterparts.
Absolute isometric torque was signiWcantly higher in the
obese group at short (+24.6%; P < 0.01) but not at long quad-
riceps muscle length (+16.4%; P > 0.05). Isometric torque
normalized to the fat-free mass did not diV er signiWcantly
between the two groups whatever the position of the knee.
Muscle fatigue
No signiWcant diV erence in voluntary torque loss was
observed between obese and lean adolescents throughout
and at the end (obese ¡52.6%; lean ¡52.2%) of the
isokinetic fatigue test (Fig. 1a). In the same way, stimulated
torque decreased similarly in the two groups during the
5-min isometric fatigue test (Fig. 1b).
Discussion
The main Wndings of the present study were that muscle
fatigue, both voluntary and stimulated, and muscle strength
per unit of fat-free mass, both isokinetic and isometric, did
not diV er signiWcantly between severely obese and nonob-
ese adolescents, therefore suggesting that obesity has little
or no eV ect on quadriceps muscle function characteristics.
We also demonstrated that maximal quadriceps strength
was produced at diV erent knee joint angles in nonobese and
obese adolescents, the latter privileging more extended
positions (shorter muscle lengths).
Muscle fatigue is deWned as an exercise-induced reduc-
tion in the ability of a muscle to generate force (Gandevia
2001) and may develop at various levels of the neuromus-
cular system. In the present study, we used two diV erent
fatigue protocols (voluntary and stimulated) to gain insight
into central and peripheral factors underlying muscle
fatigue. Since voluntary and stimulated torque decreased
similarly both throughout and at the end of the fatigue
Table 1 Fat-free mass and
muscle strength in obese and
lean adolescents
Obese Lean Obese versus
lean (%)
P
FFM (kg) 62.2 § 7.4 52.9 § 8.5 +15.0 0.009Isokinetic strength
Torque (Nm) 135.4 § 25.1 116.5 § 23.9 +16.3 0.032
Torque/FFM (Nm/kg) 2.20 § 0.38 2.20 § 0.38 ¡0.3 NS
Angle of peak torque (°) 48.1 § 6.2 53.9 § 3.4 ¡10.7 0.018
Isometric strength
40°-torque (Nm) 193.8 § 26.0 155.5 § 31.4 +24.6 0.004
40°-torque/FFM (Nm/kg) 3.15 § 0.49 2.94 § 0.32 +7.3 NS
80°-torque (Nm) 232.0 § 44.9 199.3 § 49.5 +16.4 NS
80°-torque/FFM (Nm/kg) 3.73 § 0.63 3.77 § 0.67 ¡1.0 NS
Values are mean § SD
FFM fat-free mass,
NS non signiWcant
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484 Eur J Appl Physiol (2008) 103:481–484
123
protocols in the two subject groups, there is no reason to
believe that central and/or peripheral mechanisms of mus-
cle fatigue could diV er between obese and nonobese adoles-
cents—contrary to what we have recently reported for male
adults (MaYuletti et al. 2007). Obese adults demonstrated
indeed signiWcantly greater fatigue during voluntary but not
during stimulated knee extensions compared to their lean
counterparts (MaYuletti et al. 2007). Interestingly, volun-
tary fatigue—in addition to stimulated fatigue—was com-
parable between these nonobese adults and the adolescents
tested in this study (both obese and nonobese).
Quadriceps force-generating capacity depends upon
many neural and muscular factors, such as the extent of
motor unit activation and muscle cross-sectional area. The
severely obese adolescents tested in this study produced
signiWcantly higher absolute muscle torque (both isokinetic
and isometric) than their lean counterparts, except at long
muscle length. This was mainly the result of greater fat-free
mass (and probably of greater quadriceps cross-sectional
area) in obese than in lean adolescents. The fact that muscle
strength adjusted to fat-free mass was comparable between
obese and nonobese subjects, allows one to speculate that
severe obesity in male adolescents would not aV ect intrinsic
muscle contractile properties as well as muscle activation
during maximal eV orts. Using the twitch interpolation tech-
nique, Blimkie et al. (1990) demonstrated lower quadriceps
activation in obese (body mass index 31 kg/m2; age
16.6 years) than in nonobese adolescents, however their
obese and nonobese subjects had similar absolute strength
and fat-free body mass, contrary to the adolescents evalu-
ated in our study.
Interestingly, we observed signiWcant quadriceps muscle
strength diV erences between obese and lean adolescents
related to knee joint position (as provided by the isokinetic
device), for both isokinetic and isometric tests. Althoughpossible diV erences in actual (not device) knee angle
between the two groups cannot be excluded (see Tsaopou-
los et al. 2007), we speculate that obese subjects would
present an advantage at short rather than at long muscle
length. Adolescents who are obese would probably limit
deliberately their range of motion during daily and sport
activities involving deep knee Xexion, because of excessive
stress acting on articular joint surfaces. This speciWc train-
ing stimulus would inevitably result in favorable adapta-
tions at short muscle length—which could explain the
present Wndings—but this would also engender a disadvan-
tage at long muscle length, which remains to be ascertained
in future studies.
Acknowledgments This study was partially supported by “Progetto
di Ricerca Corrente”, Istituto Auxologico Italiano, IRCCS, Milan, Ita-
ly. The authors are extremely grateful to the Auxology Division staV
(Istituto Auxologico Italiano, Piancavallo, Italy).
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Fig. 1 Mean (§SE) torque decrease during the 50 voluntary isokinet-
ic contractions (a) and during the 5-min electrical stimulation protocol
(b) in obese and nonobese adolescents
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