Eur J Appl Physiol (1990) 61:313-318
European
Voluntary strength, evoked twitch contractile properties
and motor unit activation of knee extensors in obese
and non-obese adolescent males
Cameron J. R. Blimkie 1, Digby G. Sale 1, and Oded Bar-Or 2
i School of Physical Education and Athletics, and
2 Children's Exercise and Nutrition Centre, McMaster University, Hamilton, Ontario, Canada L8S 4K1
Accepted April 17, 1990
Summary. The purpose of this study was to determine
whether neural and/or muscular factors contributed to
the inferior strength-related motor performances of
obese adolescents. Subjects were 10 non-obese (14.6%
fat) and 11 obese (32.3% fat) males matched for age
(15-18 years), level of maturity (Tanner stages IV and
V), lean body mass, and height. Peak torque (PT) was
measured during maximal voluntary isometric (IS) and
isokinetic (IK) knee extension (KE). Peak twitch torque
(TT), time to peak torque (TPT), and half-relaxation
time (HRT) of the knee extensors were elicited by per-
cutaneous electrical stimulation. The interpolated
twitch technique was used to determine the extent of
motor unit activation (% MUA) during maximal volun-
tary IS KE. Knee extensor cross-sectional area (CSA)
was determined by computed axial tomography taken
at the mid-thigh. All strength and area measurements
were made on the right side of the body. Obese subjects
had significantly (P<0.05) lower maximal voluntary IS
and IK KE strength normalized for body weight, and
significantly lower % MUA during IS KE. There were
no significant differences (P> 0.05) between groups for
absolute or normalized (for the product of muscle CSA
and height) ISPT, IKPT, and TT, knee extensor CSA,
or TPT and HRT. These results suggest that reduced
MUA and a lower strength per mass ratio (due to ex-
cess fat) are probably important contributing factors to
the poorer motor performances of the obese, especially
for complex motor tasks involving large muscle groups
and the support or moving of body weight.
Key words: Contractile properties - Knee extensor
cross-sectional area - Obesity - Motor unit activation -
Voluntary strength
Offprint requests to: C. J. R. Blimkie
ou,°a,o, A p p l i e d
Physiology
and Occupational Physiology
© Springer-Verlag 1990
Introduction
Obesity is the most prevalent pediatric condition in de-
veloped countries, with estimates ranging from 5% to
10% of pre-school children, 10% of primary school chil-
dren and 15% of adolescents (Mahoney and Klykylo
1983). Childhood obesity has been associated with re-
duced exercise capacity (Bar-Or 1983) and poor motor
performance (Bar-Or 1983; Beunen et al. 1983).
The poorer motor performance of the obese has
been attributed to the handicapping effect of the "dead
weight" of excess fat (Carpenter 1941 ; Kireilis and Cur-
eton 1947; Sills and Everett 1953; Riendeau et al. 1958;
Gutezeit 1976; Beunen et al. 1983). Results from studies
by Rehs et al. (1973), and Kitagawa and Miyashita
(1978), however, suggest that other factors besides fat
mass may account for the reduced motor performance
of the obese. These studies reported lower mechanical
power output at a heart rate of 170 beats, min-1 (PWC
170), and strength respectively, per kilogram lean body
mass, for obese children and adults. These observations
suggest that obesity may be associated with a power
and strength deficit of either neural or muscle origin,
which may act independently or conjointly with excess
fat, to reduce performance.
To our knowledge, with the exception of a recent
study of pre-pubertal and pubertal boys (Blimkie et al.
1989), there have been no other studies of the ability of
obese children or adolescents to activate skeletal mus-
cle during strength performance, only one study (Ikai
and Fukunaga 1968) of the voluntary specific tension
[force or torque per unit muscle cross-sectional area
(CSA)] of muscle during strength performance in obese
children, and no reports of the twitch force or time-
related [time to peak torque (TPT) and half-relaxation
time (HRT)] contractile properties of muscle in this
population. Each of these factors may be important in
the differentiation of strength and motor performances
among children and adolescents who vary in body fat-
ness. The purpose of this study was to determine the
importance of body fatness, neural, and muscular fac-
tors in the differentiation of knee extension (KE)
314
strength between lean and obese late pubescent and
post-pubescent (adolescent) males.
Methods
Subjects and anthropometry. Subjects were 11 obese and 10 non-
obese Caucasian adolescent males between 15 and 18 years of
age. They were free from acute and chronic disease and none had
any orthopedic condition which precluded involvement in the
study. The study was approved by the University Human Ethics
Committee and all subjects and parents gave informed consent.
Physical characteristics of the subjects are summarized in Table 1.
Body fat was assessed from the sum of four skinfolds: subscapu-
lar, supra-iliac, triceps and biceps, using the equation of Durnin
and Rahaman (1967) for adolescent males. Subjects were classif-
ied as either non-obese or obese if the sums of skinfolds corre-
sponded to estimates of less than 20% and more than 30% body
fat, respectively. This equation assumes a density of 1.10 for lean
tissue, and according to Lohman (1986) probably overestimates
percent body fat and underestimates lean body mass in children
and adolescents. Additionally, this equation was developed for
males between 12.7 and 15.7 years of age. Subjects in the present
study were on average a year older than the population from
which this equation was derived, and this may also result in a
small, but additional error in the accuracy of the percent body fat
estimates. Height was measured with a stadiometer, with subjects
standing in bare feet, and body mass with subjects wearing shorts
only.
Table 1. Selected physical and anthropometric characteristics
Age Height Body Lean body
(years) (m) mass mass
(kg) (kg)
Non-obese 16.5 1.80 63.5
(n = 10) (1.0) (0.06) (10.7) (7.3)
Obese 16.6 1.75) 94.6
(n = 11) (0.9) (0.12) (14.1) (20.5)
Values are means (SD)
* Significant difference, P < 0.05
Obese subjects were outpatients treated for overweight at the
Children's Exercise and Nutrition Centre in Hamilton. The non-
obese subjects were recruited from a local secondary school.
Level of maturity was estimated according to Tanner staging of
pubic hair development (Ross and Marfell-Jones 1982), and lean
body mass was calculated from measurements of body mass and
estimates of percent body fat.
Isometric strength. For isometric (IS) strength testing, subjects sat
on a bench with an adjustable back support (2.09 rad), with the
right leg fitted into a custom-made dynamometer (Fig. 1) instru-
mented with a strain guage. The torque signal from the strain
guage was amplified, displayed on an oscilloscope (Hewlett-Pack-
ard 1201 B), and fed to a computer (PDP-11-03) for analysis. Max-
imal voluntary KE strength (peak torque, PT) was measured at
knee joint angles of 1.57, 2.09, 2.44, and 2.79 rad (3.14 rad = full
knee extension), in random order. The testing procedure has been
described elsewhere (Blimkie et al. 1989).
Isokinetie strength. Maximal voluntary (concentric contraction)
KE strength (PT) was measured for the right leg in random order
at angular velocities of 0.52, 1.05, 2.09, and 3.14 rad-s -1, using a
Cybex II isokinetic dynamometer (Lumex, Ronkonkoma, New
York). The testing procedure has been described in detail else-
where (Blimkie et al. 1989).
Subjects completed three test trials separated by 30-s pauses
at each joint angle and velocity of contraction, respectively, for IS
and isokinetic (IK) strength testing. The average of the best two of
three trials was used as the criterion score. All strength tests were
conducted on the same day, during a 2-h period, and IS strength
testing always preceded IK testing.
Twitch contractile properties. Evoked IS contractile properties
were measured for the right knee extensors using the same dyna-
mometer as for voluntary IS strength testing. Due to the discom-
fort associated with the evoked technique when applied to large
muscle groups, these properties were measured at only the single
joint angle of 1.57 rad. To preclude the effect of twitch potentia-
tion caused by prior voluntary contraction (Vandervoort et al.
1983), the contractile properties were measured before maximal
voluntary strength. Rubber impregnated stimulating electrodes
were placed over the femoral nerve in the femoral notch (cathode)
and just proximal to the patella in the mid-line of the thigh. Peak
twitch torque (TT) was determined by applying a series of 100-p~s
square-wave pulses of increasing voltage until no further increase
in q T occurred. TPT and HRT were determined for the peak
twitch response by computer analysis (sampling rate of 500 Hz).
Motor unit activation. The degree of motor unit activation (MUA)
was determined for the right knee extensors (at 1.57 rad) using the
technique described by Belanger and McComas (1981). With this
technique, a single supramaximal electrical stimulus is applied to
Z4 Body Body mass
Skinfolds fat index
(mm) (%) (kg- m - 2)
55.7 24.1 14.6 19.6
(6.2) (3.1) (2.9)
57.1 110.4 32.3 31.0
(24.0) (1.8) (2.7)
Fig. 1. Schematic representation of the experimental procedures
for determining maximal voluntary isometric strength, evoked
contractile properties, and motor unit activation of the knee ex-
tensor muscles

a muscle at the peak of a maximal voluntary IS contraction. A
quantitative expression of the % MUA is obtained by comparing
the magnitude of the torque increment following the stimulation
(interpolated twitch torque, ITT) to that of the evoked peak TT
response:
% MUA = I T T - TT/TT x 100.
This procedure followed the measurement of the resting contrac-
tile properties, and the average of two trials was taken as the cri-
terion score.
Thigh morphology. Morphological measurements were made of
the right thigh using computed axial tomography (CT) scanning
(fourth generation high resolution, Ohio Nuclear 20/20 series
scanner). A single scan (5 mm thickness, and 15 mrem effective
radiation dose) was taken mid-way between the public symphysis
and the medial condyle of the femur, with subjects lying supine
and with the muscles relaxed. The thigh was positioned so that it
was perpendicular to the scanning window. The pubic region and
the proximal thigh were covered with a lead apron to protect
against radiation exposure. Negative photographic slides were
made from the CT scan prints and the following measurements of
CSA were made from tracings of the projected slides using com-
puter-assisted manual planimetry: total limb area, fat area, lean
area (muscle and bone), bone area, and knee extensor area.
Data transformation. Strength measurements were normalized for
(a) body mass (N m. kg- 7) and (b) the product of quadriceps CSA
and height (N m- ram-Z- m-l) _ normalization for both muscle
CSA and muscle moment arm length (mechanical advantage), the
latter assumed to be proportional to height (Sale et al. 1987).
Statistical analys&. A two-factor analysis of variance with re-
peated measures (across joint angles and velocities) was used to
determine significant effects for all strength results. A post-hoc
Tukey test was used to identify significant differences among
means. A t-test for independent measures was used to determine
the significance of differences between groups for physical, an-
thropometric and morphological characteristics. The Mann-Whit-
ney non-parametric test was used to determine the significance of
differences in MUA between groups. Differences were considered
significant at the P < 0.05 level. Pearson product-moment correla-
tion coefficients were computed to determine the relationships be-
tween quadriceps CSA and IS (at 1.57 rad), IK (at 0.52 rad.s-1),
and evoked TT (at 1.57 rad).
Results
Anthropometric characteristics
There were no significant differences b e t w e e n g r o u p s
for age, height or lean b o d y mass (Table 1). Obese sub-
Fig. 2. Computed axial tomography (CT) scans taken at the mid-thigh (right leg) of (A) obese and (B) non-obese adolescent boys
315
jects were significantly heavier a n d fatter, a n d h a d a
significantly higher b o d y mass index t h a n n o n - o b e s e
boys. Subjects were either T a n n e r stage 4 or 5, a n d the
distribution o f subjects by maturity level was equal
within groups.
Thigh morphology
Representative C T scans o f the leg for an obese a n d
n o n - o b e s e adolescent male are s h o w n in Fig. 2. Mor-
p h o l o g i c a l characteristics are presented in Fig. 3. Obese
subjects h a d significantly larger total thigh a n d fat C S A
t h a n n o n - o b e s e subjects. There were no differences in
total lean CSA, b o n e CSA, or knee extensor (quadri-
ceps) C S A between groups.
Voluntary strength
IS (Fig. 4) a n d I K (Fig. 5) strength m e a s u r e m e n t s
s h o w e d the same pattern o f results. There were no dif-
ferences between g r o u p s for either absolute strength
(panel A), or strength expressed per unit p r o d u c t o f
quadriceps C S A a n d height (panel C); however, the
obese boys h a d significantly ( P < 0.05) lower IS a n d I K
strength expressed per kilogram b o d y mass (panel B).
Contractile properties
Despite slightly higher values for the obese, there
were no significant differences ( P > 0 . 0 5 ) b e t w e e n
g r o u p s for absolute T T [39.1 (7.8) vs 43.5 (12.7) N m ;
m e a n (SD)], T T n o r m a l i z e d for the p r o d u c t o f quadri-
ceps C S A and height [0.0032 (0.001) vs 0.0038 (0.001)
N m . m m - Z . m - 1 ] , T P T [70.5 (7.9) vs 75.5 (17.9) ms] or
H R T (56.4 (28.4) vs 65.3 (20.4) ms].
Motor unit activation
The obese subjects h a d a significantly ( P < 0 . 0 5 ) lower
m e a n degree o f M U A (85.1 vs 95.3%) a n d a m o r e varia-
ble response (71-100% vs 89-100%) t h a n the n o n - o b e s e
g r o u p during m a x i m a l v o l u n t a r y IS KE.
316

MID - THIGH ISOKINETIC STRENGTH

h" 250 0--0 NON-OBESE
30x10 a. e--e OBESE
E
g
,¢ 200

t/
l,U F//A
re
--I 20x10 a. 150
<
z
2 1oo
I-
O
10x10 s.
I 50
m 4
o
re
O f
t- 3
O
TOTAL FAT LEAN BONE EXTENSOR
AREA AREA AREA AREA AREA

Fig. 3. Morphological characteristics of the right mid-thigh of

obese ( ~ ) and non-obese (El) adolescent males determined from E
t
CT scans. Values are means (ram 2) and SD. * Significant differ-
ence (P< 0.05) between groups
0
.03,
ISOMETRIC STREN6TH
300 A
o ONONOBESE
250 I I • • OBEBE .02

200
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E
150 t: E
.01

co
t-1 100

50
I o
0.52 1.05 2.09 3.14
CONTRACTION VELOCITY (Pad.s-t)

3
!
0-'
T Fig. 5A-C. Peak voluntary isokinetic strength of the knee exten-
sors at contraction velocities of 0.52, 1.05, 2.09, and 3.14 rad. s -
for adolescent obese and non-obese males. A Absolute torque
(N m). B Relative torque (N m.kg -~) - absolute torque normal-
ized for body mass. C Voluntary specific tension
(N m.mm-Z-m -a) - absolute torque normalized for quadriceps
E
co 1 cross-sectional area and height. Values are means (SD). * Signifi-
H
1 cant (P<0.05) main effect for groups. IKPT, Isokinetic peak tor-
que
0

.03

Correlational relationships
.02
?
T h e results for the c o r r e l a t i o n a l a n a l y s e s are p r e s e n t e d
i n T a b l e 2. D u e to the small samples, n o n e of the w i t h i n
-- .01
t g r o u p c o r r e l a t i o n s was s i g n i f i c a n t ( P > 0.05). N e v e r t h e -
E
O3
H
less, the c o r r e l a t i o n s were c o n s i s t e n t l y h i g h e r i n the
o n o n - o b e s e t h a n the obese group, a n d w i t h i n each g r o u p
1.57 2.09 2.44 2.79 were h i g h e r for v o l u n t a r y p e a k IS s t r e n g t h t h a n for
JOINT ANGLE (rad) either p e a k I K strength, or TI'. W h e n the g r o u p s were
c o m b i n e d , p r o v i d i n g a larger s a m p l e , there were signif-
Fig. 4A-C. Peak voluntary isometric strength of the knee exten- icant (P<0.05) moderate correlations between quadri-
sors at 1.57, 2.09, 2.44 and 2.79 rad for adolescent obese ( 0 - - 0 ) ceps C S A a n d b o t h p e a k IS strength a n d T-I'.
and non-obese ( O - - O ) males - 3.14 rad is full extension. A Ab-
solute torque (N m). B Relative torque (N m.kg -~) - absolute
torque normalized for body mass. C Voluntary specific tension Discussion
(N m. mm - 2. m - i) _ absolute torque normalized for quadriceps
cross-sectional area and height. Values are means (SD). * Signifi-
cant (P<0.05) main effect for groups. ISPT, Isometric peak tor- I n the p r e s e n t study, there were n o differences i n abso-
que lute IS a n d I K K E strength, or IS a n d I K K E v o l u n t a r y

Table 2. Pearson product-momentcorrelations between peak vol-
untary isometric and isokinetic strength, evoked twitch torque,
and knee extensor (quadriceps) cross-sectional area (CSA)
Groups
Non-obese Obese Combined
Isometric peak torque
(1.57 rad) and 0.555 0.453 0.512"
quadriceps CSA (n = 10) (n = 10) (n = 20)
Isokinetic peak torque
(0.52 rad.s -1) and 0.455 0.387 0.281
quadriceps CSA (n = 10) (n = 11) (n = 21)
Twitch torque (1.57 rad) 0.398 0.167 0.457*
and quadriceps CSA (n = 10) (n = 10) (n = 20)
* Statistically significantat P< 0.05
specific tension between obese and non-obese adoles-
cent males. The obese adolescents however, had signifi-
cantly lower strength per unit mass and reduced MUA
compared to the non-obese. These results indicate that
the handicap of excess fat mass in conjunction with re-
duced neuromuscular activation may account for the
lower strength per mass ratio observed in the obese
subjects in the present study, and the reported reduced
motor performance typical of obese children and ado-
lescents (Bar-Or 1983; Beunen et al. 1983) and adults
(Kitagawa and Miyashita 1978; Sills and Everett
1953).
Previous studies have demonstrated moderate to
strong positive correlations between maximal voluntary
IS strength and muscle CSA in adults (e.g., Ikai and
Fukunaga 1968; Maughan et al. 1983) and in children
(Ikai and Fukunaga 1968; Davies et al. 1983; Davies
1985), and between muscle CSA and TT in mammals
(Close 1972). These observations suggest that muscle
size is an important determinant of both voluntary and
evoked muscle strength. Correlational analyses indi-
cated that quadriceps CSA had a significant, albeit only
a moderate influence, on voluntary IS strength and
evoked TT in this study. These results confirm that
muscle size is an important determinant of voluntary
and evoked IS force development during adolescence.
The magnitude of the correlations suggest, however,
that other factors besides muscle CSA may be impor-
tant in the determination of large muscle-group
strength, especially IK strength, and that the relative
importance of muscle CSA in determining quadriceps
strength may vary with level of adiposity in adolescent
males.
With the exception of the reports by Blimkie (1989)
and Blimkie et al. (1989), there are no other studies to
our knowledge of voluntary or evoked specific tension
of the KEs of children. Kitagawa and Miyashita (1978)
reported no significant difference in relative (per kilo-
gram lean body mass) KE strength between mildly
obese and non-obese adult males. While lean body
mass is anindirect and less precise indicator of muscle
size than measured CSA, their results appear to support
both our recent (Blimkie et al. 1989) and current find-
317
ings, and indicate that there is no deficit in voluntary or
evoked specific tension of KEs associated with obesity
in males during either the circumpubertal years or early
adulthood. These results suggest that the lower strength
per mass and poorer strength-related motor perform-
ances of the obese are probably not due to differences
in intrinsic contractile properties of muscle.
Voluntary specific tension is determined in part by
level of neuromuscular activation. It appears from the
MUA results that the obese subjects, with an equally
high level of motivation and effort (determined subjec-
tively), were not as capable as the non-obese group of
voluntarily activating the quadriceps during the rather
simple and unskilled task of IS KE. Yet, despite this
relative inhibition of muscle activation, there was no
difference between groups for voluntary KE-specific
tension. Although speculative, perhaps the obese could
have achieved a higher level of voluntary specific ten-
sion, had they been capable of more fully activating
their motor unit pool.
It is difficult to explain the similarity in voluntary
specific tension between groups, given the lack of dif-
ference in twitch-specific tensions, and the significantly
lower % MUA for the obese subjects. One possible ex-
planation would be a higher intrinsic specific tension
(force per CSA) in the obese group during maximal vol-
untary efforts, which was not detected using TT meas-
urements, but which may have been revealed from te-
tanic torque measurements. An increased contribution
of synergistic muscle action in the obese would be an-
other possibility. Increased synergistic muscle involve-
ment would increase voluntary force output and the
voluntary specific tension, without influencing the in-
terpolated twitch and MUA responses. Why the obese
would rely more heavily on the greater involvement of
synergistic muscles, in the absence of muscle damage or
disease, to execute such a simple task, remains un-
clear.
It was impossible, with the techniques used in this
study, to determine the cause of the reduced MUA
among the obese. Given the simplicity of the maneuver,
and the apparent maximal effort during the task, it
seems unlikely that reduced motivation or central drive
was a contributing factor. Perhaps some undescribed
neural mechanism, of either afferent or efferent origin,
may account for this inhibition. Regardless of its origin,
it is possible that reduced neuromuscular activation
might preclude full realization of strength capacity in
the obese, and thereby contribute to the motor perform-
ance deficit evident in this group for more complex ac-
tivity patterns, especially those involving large muscle
groups and a high degree of leg muscle strength.
Thoren et al. (1973) have suggested that the extra
weight carried by the obese might serve as a favorable
training stimulus. Bosco et al. (1986) have reported sig-
nificant increases in muscle power in athletes who con-
tinued to train, while wearing weight vests. If the
weight of the vest is considered analogous to the excess
dead weight of fat in obesity, then these results would
appear to support Thoren's position. The additional
weight of excess fat did not, however, significantly in-
 318
c r e a s e m u s c l e size, v o l u n t a r y s t r e n g t h o r s p e c i f i c ten-
s i o n o f t h e K E s f o r t h e o b e s e s u b j e c t s in t h e p r e s e n t
study. F a v o r a b l e a d a p t a t i o n s to excess fat m i g h t b e de-
p e n d e n t u p o n t h e s u s t e n a n c e o f s u f f i c i e n t levels o f h a -
b i t u a l p h y s i c a l activity, a c o n d i t i o n w h i c h a c c o r d i n g to
s o m e (e.g., B u l l e n et al. 1964; D u r n i n 1971), b u t n o t
o t h e r s (e.g., H u t t u n e n et al. 1986; W i l k i n s o n et al.
1977), is n o t a l w a y s m e t b y o b e s e c h i l d r e n o r a d o l e s -
cents.
I n c o n c l u s i o n , t h e results o f this s t u d y s u g g e s t t h a t
the poorer strength-related motor performances of
o b e s e a d o l e s c e n t m a l e s are p r o b a b l y n o t d u e to differ-
ences in t h e i n t r i n s i c c o n t r a c t i l e c h a r a c t e r i s t i c s o f m u s -
cle, b u t m a y b e d u e , in p a r t , to a r e l a t i v e i n h i b i t i o n o f
M U A , e s p e c i a l l y d u r i n g activities w h i c h i n v o l v e f a i r l y
large m u s c l e g r o u p s s u c h as the k n e e e x t e n s o r s . I n m o -
t o r t a s k s w h i c h r e q u i r e lifting or s u p p o r t o f o n e ' s b o d y
w e i g h t , e x c e s s fat is p r o b a b l y t h e m o s t i m p o r t a n t h a n -
d i c a p p i n g i n f l u e n c e for t h e o b e s e child. H o w e v e r , o t h e r
factors, i n c l u d i n g d i f f e r e n c e s in m o t i v a t i o n , skill, c o o r -
d i n a t i o n a n d M U A p r o b a b l y also c o n t r i b u t e to t h e re-
d u c e d m o t o r p e r f o r m a n c e o f the o b e s e a d o l e s c e n t , es-
pecially during more complex and physiologically de-
m a n d i n g m o t o r tasks.
Acknowledgements. This study was supported by a grant from the
A r t s Research Board, McMaster University. The authors thank
Joan Martin, Marg Sterling, and Sandra Enright for assisting with
the data collection; Mr. Bob Foot and his students from Parkside
Secondary School; and the patients from the Children's Exercise
and Nutrition Centre, Hamilton, for their co-operation and parti-
cipation in this study. Special thanks go to Dr. Duncan MacDou-
gall for his encouragement and support, and to Sharron Kennedy
for assisting with the typing of the manuscript.
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