Gait & Posture 56 (2017) 100–107

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Gait & Posture

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Review

Potential contributions of skeletal muscle contractile dysfunction to altered MARK

biomechanics in obesity
⁎
Lance M. Bollinger
Department of Kinesiology and Health Promotion, University of Kentucky, Lexington, KY, United States

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Obesity alters whole body kinematics and joint kinetics during activities of daily living which are
Strength thought to contribute to increased risk of musculoskeletal injury, development of lower extremity joint
Specific force osteoarthritis (OA), and physical disability. To date, it has widely been accepted that excess adipose tissue
Power mass is the major driver of biomechanical alterations in obesity. However, it is well established that obesity is a
Fatigue
systemic disease affecting numerous, if not all, organ systems of the body. Indeed, obesity elicits numerous
Muscle mass
adaptations within skeletal muscle, including alterations in muscle structure (ex. myofiber size, architecture,
lipid accumulation, and fiber type), recruitment patterns, and contractile function (ex. force production, power
production, and fatigue) which may influence kinematics and joint kinetics. This review discusses the specific
adaptations of skeletal muscle to obesity, potential mechanisms underlying these adaptations, and how these
adaptations may affect biomechanics.

1. Background reduced individuals remain at substantially higher risk of physical

Obesity directly afflicts over one-third of American adults [1] and
induces numerous kinematic alterations during activities of daily living
(ADLs) [2–5] which are thought to contribute to development of
musculoskeletal injuries [4,6], lower extremity osteoarthritis (OA)
[7–9], and physical disability [10–13]. Indeed, it has been estimated
that for every kg increase in body mass, risk of OA increases by up to
13% [14]. Numerous studies have examined the effects of obesity on
biomechanics during various ADLs [2–4,7,15–22]. These studies have
largely focused specifically on the effects of obesity on lower extremity
kinematics and kinetics during gait, and to a lesser extent, rising from a
chair. The specific kinematic and kinetic adaptations to obesity during
these ADLs have been reviewed previously [23] and are summarized in
Table 1. The purpose of this review is to discuss skeletal muscle
adaptations to obesity, potential mechanisms underlying these adapta-
tions, and how these may contribute to altered biomechanics.
Currently, weight loss is the major recommended intervention for
improving biomechanics and reducing risk of joint injury, OA, and
disability in obesity. However, a recent meta-analysis of 18 wt loss
studies (N = 1636) indicates that 3–24 months of intervention resulted
only in 4.9 kg (diet alone) and 6.7 kg (diet + exercise) weight loss
which corresponded to 1.9 and 2.5 kg/m2 reduction in body mass index
(BMI), respectively [24]. Although this degree of weight loss will likely
decrease risk of complications of obesity, it is likely that weight-
disability and lower extremity OA than their normal weight peers.
Furthermore, weight regain is common following weight loss interven-
tions [24]. Indeed, Kramer et al. [25] reported that less than 3% of their
152 subjects maintained their reduced body mass five years after a 15
wk weight loss intervention. Therefore, weight loss interventions are
unlikely to completely ameliorate risk of developing injury or OA,
especially in long-term interventions. Therefore, it is imperative to
explore and understand mechanisms other than body mass per se which
may contribute to obesity-induced biomechanical alterations.
2. Effects of obesity on skeletal muscle contractile function
In addition to increasing body mass, obesity elicits numerous
skeletal muscle adaptations including altered contractile function
(force, power, and fatigue), muscle structure (myofiber size, architec-
ture, lipid accumulation, and fiber type), and recruitment patterns.
Table 2 summarizes previously published effects of obesity on skeletal
muscle.
2.1. Skeletal muscle strength
Absolute muscle strength is increased in obesity [26–31], at least in
younger adults. Indeed, it has previously been suggested that increased
muscle strength is a beneficial adaptation to obesity [29]. It should be

⁎
Correspondence author at: University of Kentucky, 201 Seaton Bldg., Lexington, KY 40506, United States.
E-mail address: Lance.bollinger@uky.edu.

http://dx.doi.org/10.1016/j.gaitpost.2017.05.003
Received 3 January 2017; Received in revised form 4 May 2017; Accepted 6 May 2017
0966-6362/ © 2017 Elsevier B.V. All rights reserved.
L.M. Bollinger Gait & Posture 56 (2017) 100–107

Table 1
Previously reported biomechanical adaptations to obesity. Previous studies examining biomechanics during gait and sit-to-stand are presented. The effect of obesity (relative to lean) and
the approximate magnitude of the effect of obesity is indicated. O = obese; L = lean; GRF = ground reaction forces; sag = sagittal plane.

Study Activity Subjects Outcomes Effect of Obesity Magnitude of Effect

Browning Treadmill walking Lean Obese GRF O > L 60%

and Kram (0.50–1.75 m/s) BMI 20–25 BMI 30–43 Stance duration O > L 5–7%
Med Sci Age: 25–32 Age: 25–32 Double support O > L 15–20%
Sports Exerc n = 10 n = 10 Swing time O < L 7–15%
2007 [10] Step width O > L 30%
Joint angles O=L 70%
Hip moment (sag) O > L 50%
Knee moment (sag) O > L
Ankle moment (sag) O=L

DeVita and Overground Lean Obese Stance duration O > L 3%

Hortobagyi Walking BMI 16–27.3 BMI 32.4–58.7 Swing time O < L 5%
J Biomech (Self-selected pace) Age 20.8 Age 39.5 Hip extension O > L 5°
2003 [17] n = 18 n = 21 Knee extension O > L 4°
Ankle plantarflexion O > L 5.5–7.5°

Lai et al. Overground Lean Obese Walking speed O < L 12%

Clin Biomech walking BMI 21.3 BMI 33.1 Stride length O < L 8%
2008 [41] (Self-selected pace) Age 27.6 Age 35.4 Stance duration O > L 3%
n = 14 n = 14 Double support O > L 18%
Hip adduction O > L 3°
Knee adduction O > L 4.5–8°
Ankle eversion O > L 5°

Lerner et al Treadmill walking Lean Obese Pelvis obliquity O > L N/A

Gait Posture (1.25 and 1.50 m/s) BMI 22.1 BMI 35.0 Hip extension O=L N/A
2014 [43] Age 26 Age 35 Knee extension O > L
n = 10 n=9

McMillan et al. Overground Lean Obese Hip extension O > L 8–12°

Gait Posture walking BMI 20.3 BMI 44.6 Hip abduction O=L 6°
2010 [50] (Self-selected pace) Age 12–17 Age 12–17 Knee extension O > L 6–9°
n = 18 n = 18 Knee abduction O > L 3°
Ankle plantarflexion O > L 2°
Ankle eversion O < L 0.15–0.29 Nm/kgm
Hip flexion moment O > L 0.7–0.13 Nm/kgm
Hip adduction moment O > L 0.8–0.20 Nm/kgm
Knee extension moment O > L 0.15 Nm/kgm
Knee adduction moment O > L 0.20 Nm/kgm
Ankle dorsiflexion O > L 0.04 Nm/kgm
Ankle eversion O > L

Spyropoulos et Overground Lean Obese Walking speed O < L 33%

al. walking Age 30–47 (70–99% ideal Stride length O < L 25%
Arch Phys (Self-selected pace) n = 12 Body mass) Step width O > L 200%
Med Rehabil Age 30–47 Hip flexion O=L N/A
1991 [74] n = 12 Hip abduction O < L N/A
Knee flexion O=L
Ankle dorsiflexion O > L

Galli et al. Sit-to-stand Lean Obese Trunk flexion O > L 17°

Int J Obes BMI 22 BMI 40 Hip moment O < L 0.240 Nm/kgm
2000 [22] Age 28.0 Age 39.4 Knee moment O > L 0.437 Nm/kgm
n = 10 n = 30

Huffman et al. Sit-to-stand Lean Obese Sit-to-stand duration O=L 5°

Gait Posture BMI 22.1 BMI 31.2 Trunk flexion O=L 0.073 Nm/kgm
2015 [32] Age 24.9 Age 33.4 Hip flexion O=L 0.204 N
n = 10 n=9 Hip abduction O > L
Hip abduction moment O > L
Medial GRF O > L

Schmid et al Sit-to-stand Lean-overweight Obese Peak velocity O < L 23%

J Appl Biomech BMI < 17.5–29.9 BMI > 30, > 35 Mean velocity O < L 20%
2013 [68] Age: 50.9 Age: 48.9, 48.5 Total time (5 cycles) O > L 37%
n = 10 n = 10, 16 Toe-out angle O=L
Interheel distance O=L

Sibella et al. Sit-to-stand Lean Obese Trunk flexion O < L 24°

Clin Biomech BMI 23.0 BMI 37.9 Hip moment O < L 0.40 Nm/kgm
2003 [72] Age 26.5 Age 48.5 Knee moment O > L 0.37 Nm/kgm
n = 10 n = 40

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L.M. Bollinger Gait & Posture 56 (2017) 100–107

Table 2
Previously reported effects of obesity on skeletal muscle contractile function. The effect and approximate magnitude of effect of obesity on skeletal muscle contractile function from
previously published papers is presented. In order to distinguish between effects of obesity and age, results are separated by subject age. O = obese; L = lean.

Muscle Function Parameter Adaptation to Obesity Magnitude of effect Supporting Reference(s)

Strength Absolute strength Young O > L 10–30% [2,23,33,40,47,58,80,81]

Old O≥L 7–18% [13,62,80][13,62,80,89]
Relative strength Young O < L 6–43% [2,7,33,47,58,80]
Old O < L 15–43% [13,80]
Intrinsic/Specific force Young O < L 25–40% [81]
Old O < L 25–40% [13]

Power Absolute power Young O > L 10–32% [39,47]

Old O > L 24% [39]
Relative power Young O < L 18–32% [40,47]
Old O < L 50% [13,39]

Fatigue Volitional fatigue Young O > L 25% [47]

Old ??
Stimulated fatigue Young O=L ND [47]
Old ??

Muscle mass Absolute muscle mass Young O > L 12–50% [23,58,81,82]

Old O > L 30% [13,82]
Fiber size Young O > L 20% [23,25]
Old O > L 10% [13]

Fiber type Type I MHC Young O < L 35% [8,79]

Old ??
Type II MHC Young O > L 75% [38,79]
Old ??

Architecture Pennation angle Young O > L 24% [23,82]

Old O > L 20% [82]

Neural activation Agonist EMG Young O < L 10% [7,80]

Old O=L ND [80]
Agonist/antagonist Young O=L ND [80]
Co-activation Old O=L ND [80]

noted that obese older adults do not necessarily display increased
absolute muscle strength as their younger counterparts do [11,27].
However, Rolland et al. [32] noted that physically active (> 1 h/wk)
obese older adults displayed increased absolute knee extension strength
(198.4 N) than their lean (168.0 N) or obese (169.0 N) sedentary
counterparts. Therefore, it is possible that physical activity may provide
a muscle overload stimulus and may be a requirement for increased
absolute strength in obesity.
Several papers have demonstrated increased absolute strength
(approximately 10–30%) during knee extension exercise in obesity
[26,29,31]. However, it is less clear whether this increase in muscle
strength is specific only to anti-gravitational muscles. Lafortuna et al.
[28] evaluated muscle strength of lower extremity (leg press one
repetition maximum) and upper extremity muscles (chest press) in
lean and severely obese subjects. Compared to lean, severely obese
subjects were 32% (men) and 23% (women) stronger during lower
extremity testing. However, no difference in muscle strength was
observed for upper extremity muscles suggesting that excess body mass
may elicit an overload response to increase muscle strength specifically
of anti-gravitational muscles. In contrast, Pescatello et al. [33] found
that strength of the elbow flexors was approximately 20% higher in
overweight and obese adults suggesting that obesity per se increases
muscle strength independent of an overload stimulus. It should be
noted that both these studies examined subjects who did not regularly
engage in physical activity. Therefore, it is unlikely that exercise-
induced muscle overload contributed to the findings in these papers.
Rolland et al. [32] noted that absolute knee extension (181.2 v.
169.4 N) and elbow flexion (102.8 v. 93.5 N), but not handgrip
(52.2 v. 50.6 N), strength was higher in obese v. lean older adults.
When adjusted for physical activity, knee extension, elbow flexion, and
handgrip strength were all significantly higher in obese v. lean subjects
suggesting that physical activity may mediate some of the effects of
obesity on skeletal muscle strength.
Hulens et al. [31] noted increased absolute strength for knee
extension (11.5%), trunk extension (10.7%), trunk flexion (28.7%),
and trunk rotation (6.6%) in obese women. However, these researchers
found no difference in handgrip or knee flexion strength between lean
and obese subjects. Based on these findings, it is unclear whether
increased absolute muscle strength in obesity is limited solely to anti-
gravitational muscles. It may be that skeletal muscle strength is
increased in a muscle-specific manner in obesity. Obesity may elicit
biomechanical adaptations that favor use of these stronger muscle
groups and minimizes workload of weaker muscle groups. For example,
during gait, obese subjects tend to walk with a shorter stride length
(0.71 v. 0.77 m/m height) and increased time in stance (60.21 v.
58.51% gait cycle) and double support (11.29 v. 9.55% gait cycle)
[21]. This strategy would be expected to increase workload on the knee
extensors and decrease workload on the hamstrings. Indeed, Amiri et al.
[34] noted that, in addition to slower walking pace and longer time
spent in stance phase during gait, obesity was associated with pro-
longed activation of the quadriceps, but not hamstring muscles.
Since many ADLs require translocation of the entire body through
space, skeletal muscle strength relative to body mass may be an
important determinant of mobility. Although absolute muscle strength
is generally increased in obesity, when normalizing muscle strength to
total body mass, it is apparent that relative muscle strength is decreased
in obesity. Several groups have reported that relative knee extensor
muscle strength is approximately 20–30% lower in obesity
[26,30,35,36].
Not only is it clear that skeletal muscle strength relative to body
mass is decreased in obesity, but recent evidence suggests that the
intrinsic ability of skeletal muscle to produce force is decreased in
obesity [27,30,31,37]. When adjusting for fat-free mass, Hulens et al.
[31] found muscle strength was 6–20% lower in obese vs. lean subjects
for several muscle groups. Tomlinson et al. [27] expounded upon this
finding when they showed obese individuals displayed lower intrinsic

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L.M. Bollinger
(force/muscle volume, −26%) and specific (force/physiological cross-
sectional area, −34%) plantarflexion force than their normal weight
counterparts. Choi et al. [30] reported a similar ∼35% decrease in
intrinsic force of the knee extensors of older obese women compared to
lean women of similar age. These authors further reported that maximal
calcium-stimulated force production (25–35%) was decreased in iso-
lated muscle fibers (both type I and IIa fibers) of obese women.
However, this effect was more pronounced in type I fibers. Ciapaite
et al. [38] examined muscle force production in the EDL and soleus
muscles following 5 weeks of high fat diet-induced obesity. Relative
peak twitch force production was unaltered in the EDL, but significantly
decreased (35%) in the soleus following five weeks of treatment. Since
the EDL is comprised primarily of type IIx/IIb fibers and the soleus is
composed primarily of type I/IIa fibers, it is possible that obesity alters
skeletal muscle force production in a fiber type specific manner. These
data suggest that obesity directly impairs the ability of skeletal muscle
to produce force, especially in type I fibers. Decreased muscle strength
in obesity may have important implications for physical function as it is
well established that obesity-induced mobility impairments are com-
pounded by low levels of muscle strength [39].
Muscle weakness is associated with increased joint loads [40] and
development of knee OA (quadriceps) [41] and low back pain (spinal
flexors) [42]. Simulating muscle weakness of the vastus medialis
induces a lateral patellar shift in cadavers [43] indicating that muscle
weakness alone is sufficient to alter joint kinematics. In order to
determine the effects of muscle weakness on knee mechanics, Murdock
et al. [44] studied gait patterns before and after a fatiguing quadriceps
exercise session (50 maximal knee extensions at 90°/s) which reduced
quadriceps torque by 40% and power by 15%. Following this fatiguing
exercise, principle component analysis revealed a significant increase in
knee adduction angle principal component (PC1) score, primarily
during swing phase, and a significant decrease in knee rotational angle
PC1 score, indicating a more externally rotated tibia relative to the
femur. Based on these findings, it is possible that a 40% reduction in
quadriceps strength may elicit biomechanical adaptations which in-
crease risk of acute injury of development of OA at the knee joint.
Therefore, quadriceps muscle weakness may, in part, explain the 4.5-8°
increase in knee adduction angle observed by Lai et al. [21]. Future
research studies should prospectively study obese individuals with low
and high levels of relative skeletal muscle strength to determine the
specific role of relative skeletal muscle weakness in obesity-induced
biomechanical alterations.
High levels of knee extensor strength are associated with a
decreased risk of femoral-tibial joint space narrowing [45]. Further-
more, muscle strengthening improves kinematics and reduces pain in
women with patellofemoral pain syndrome [46]. Therefore, it is
possible that increasing skeletal muscle strength, particularly of the
knee extensors, may combat some of the negative effects of obesity on
knee structure and pain. It is well established that combined weight loss
and exercise improves kinematics and joint kinetics in obesity [47]. To
date, the specific effects of increasing muscle strength on kinematics
and joint kinetics in obesity have not been determined. Wang et al. [48]
demonstrated that both absolute (25%) and relative knee extensor
strength increased (37%) following a six month diet and exercise-
induced weight loss intervention in older obese adults with knee OA.
However, these authors did not report any data regarding improve-
ments in knee structure or pain reduction. Future research should
examine how increasing muscle strength – independent of weight loss –
affects kinematics and joint kinetics during ADLs. Compared to base-
line, skeletal muscle strength (leg press one repetition maximum) is
increased following three weeks of diet- and exercise-induced weight
loss [49] with little change seen in muscle mass suggesting that neural
adaptations to short term resistance training are maintained in obesity.
Short term RT interventions such as this may allow researchers to
determine the relative effects of increasing muscle strength (as opposed
to increasing muscle mass) on biomechanics.
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Gait & Posture 56 (2017) 100–107
2.2. Skeletal muscle power
Similar to skeletal muscle strength, obesity increases absolute
muscle power output, but decreases muscle power output per unit
body mass. Maffiuleti et al. [26] reported that absolute isokinetic knee
extensor power was approximately 20% higher in obese compared to
lean men, especially at fast (180°/s) contraction velocities. However,
when normalized to total body mass, knee extensor power was
approximately 33% lower in obese subjects. Due to the nature of many
ADLs, muscle power production in complex, multi-joint movements is
likely a more important contributor to mobility and functional inde-
pendence than knee extension power alone. In order to determine the
effects of obesity on skeletal muscle power during a multi-joint move-
ment, LaFortuna et al. [28] measured muscle power during five
consecutive squat jumps and determined there was no significant
difference in absolute skeletal muscle power between lean and obese
subjects. However, muscle power relative to total body mass was 40%
lower in the obese group. Furthermore, these researchers reported that
power production relative to fat free mass tended to be lower (5–15%,
p = 0.059) in obese subjects, suggesting that obesity impairs skeletal
muscle power production. In support of this, Choi et al. [30] reported
that maximal shortening velocity and power of isolated type I, but not
type II, skeletal muscle fibers was decreased in obese older adults
compared to their age-matched peers indicating that obesity indeed
impairs the ability of slow twitch fibers to produce power.
It is well established that skeletal muscle power is an important
determinant of mobility and functional capacity in older adults [50]. By
definition, muscle power is the ability to produce force rapidly;
therefore, it is possible that decreased muscle power output may
contribute to decreased speed of ADLs. Compared to lean adults, obese
individuals walk with 12 to 33% slower self-selected walking speed
[21,22]. Schmid et al. [19] reported that time to complete 5 con-
secutive sit-to-stand cycles was significantly greater (10.94 v. 7.98 s) in
subjects with a BMI > 35 compared to those with BMI < 30 kg/m2.
These authors further speculated that this impaired performance was
likely due to a combination of decreased peak force per body mass
(1.07 v. 1.26 N) and decreased rate of force development (6.79 v.
11.29 N/body mass/s) in obese subjects. Skeletal muscle power is
closely related to physical functioning [51] and incidence of falls
[52] in older adults. Therefore, impaired skeletal muscle power may
have a greater effect on physical performance as obese adults age.
2.3. Skeletal muscle fatigue
In addition to decreased relative strength and power, it has also
been reported that volitional fatigue of skeletal muscle is increased in
obesity. Maffiuletti et al. [26] demonstrated that torque loss during 50
voluntary maximal isokinetic (180°/s) knee extensions was significantly
greater in severely obese vs. lean adults. However, it should be noted
that Maffiuletti et al. [26] demonstrated no difference in isokinetic
torque loss between lean and obese during an electrically-stimulated
protocol suggesting that increased volitional muscle fatigue may be due
primarily to central, rather than peripheral, fatigue. It is possible that
this apparent increase in central fatigue is due to physical decondition-
ing from habitual physical inactivity often associated with obesity.
Skeletal muscle fatigue, even with contraction intensities < 10% MVIC
may increase reliance on synergistic muscles [53–55] and contribute to
biomechanical alterations. It has previously been reported that knee
external rotation and adduction moments are increased following a
fatiguing bout of knee extension exercise [44]. Therefore, it is possible
that skeletal muscle fatigue may contribute to increased knee adduction
angles during the swing phase of gait [21].
L.M. Bollinger
Fig. 1. Potential mechanisms by which muscle contractile dysfunction influences biomechanics in obesity. Obesity induces numerous physiological and structural alterations which
decrease relative strength and power and increase volitional fatigue. This diagram provides a framework to illustrate the potential mechanisms by which obesity impairs muscle
contractile function.
3. Effects of obesity on skeletal muscle structure
3.1. Skeletal muscle mass
In normal weight adults, skeletal muscle accounts for approximately
40% of total body mass. It has long been recognized that obesity is
associated with increased absolute levels of skeletal muscle mass
[56,57]. Indeed, in 1964, Morse and Soeldner [57] determined that
non-adipose mass (a surrogate for skeletal muscle mass) was increased
in obese, compared to lean, women. In the decades since this discovery,
several papers have shown that absolute levels of fat free mass [28],
anatomical cross sectional area (ACSA) [29], and muscle fiber CSA
[30,58] are increased in obesity. In fact, it appears that absolute levels
of fat-free mass (FFM) [28,57] and skeletal muscle mass [56] increase
with severity of obesity. Increased skeletal muscle mass may counteract
decreased specific force in obesity.
It is widely accepted that obesity increases skeletal muscle mass due
to an overload effect of excess adipose tissue. Indeed, it has previously
been observed that muscle mass increases with total body mass in a
curvilinear fashion [59]. However, there appear to be conflicting data
as to whether obesity specifically increases skeletal muscle mass solely
of load bearing muscles. BMI is independently associated with in-
creased muscle mass of the thighs, but not the arms [60], suggesting
that obesity may preferentially increase skeletal muscle mass of load-
bearing muscles. It has previously been reported that gastrocnemius
[27] and knee extensor [30] muscle mass is increased in obesity.
However, these studies did not examine mass of non-load bearing
muscles. Ciapaite et al. [38] reported that short term high fat diet-
induced obesity increased skeletal muscle mass of the soleus, but not
EDL muscles in mice, suggesting that increased muscle mass is limited
to load bearing muscles. It is possible that high levels of fat mass may
act as a resistance-training stimulus during physical activity which
induces hypertrophy of load bearing muscles. Due to the excess body
mass which must be translocated during physical activity, it is likely
that severely obese individuals may receive some level of overload
stimulus even with low levels of physical activity. In contrast, Pesca-
tello et al. [33] reported that MRI-assessed biceps brachii CSA was
approximately 19% higher in sedentary overweight and obese adults
compared to those of their normal weight counterparts. Similarly,
Rolland et al. [32] reported that appendicular skeletal muscle mass of
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Gait & Posture 56 (2017) 100–107
both the legs and arms was higher in obese older adults than their lean
or normal weight counterparts. It should be noted, however, that in
obesity, the increase in fat mass greatly exceeds the increase in FFM
[28,57] and skeletal muscle mass [38] indicating that skeletal muscle
makes up a smaller percentage of total body mass in obesity. This
decrease in relative muscularity may explain, in part, the decrease
relative strength seen in obesity.
3.2. Skeletal muscle architecture
In addition to increases in skeletal muscle mass, it has recently been
reported that obesity modifies skeletal muscle architecture by increas-
ing fascicle pennation angle (FPA) [29,61]. Tomlinson et al. [61] noted
that FPA of the medial gastrocnemius was approximately 20–25%
higher at rest and during maximal isometric plantarflexion in obese,
compared to lean, women. Furthermore, FPA was found to be sig-
nificantly correlated with body mass, suggesting that FPA increases
with severity of obesity. Increased skeletal muscle FPA of knee
extensors and plantar flexors has been also been reported in obese
adolescent girls [29], suggesting that muscle architectural changes may
be a relatively early adaptation to obesity. Resistance training is known
to increase FPA [62–64] which is likely a mechanism to increase
number of sarcomeres in parallel and, hence, increase physiological
cross-sectional area (PCSA) and force production of skeletal muscle.
Therefore, it is possible that increased FPA is an adaptive mechanism to
increase force production due to chronic skeletal muscle overload from
excess body mass or to combat the effects of decreased specific force
[27,30] seen in obesity. Vermathen et al. [65] found a positive
association (R = 0.79) between relative intramyocellular lipid (IMCL)
content and muscle fiber pennation angle in the muscles of the calf.
Therefore, it is possible that increased FPA in skeletal muscle of obese
persons is due to accumulation of non-contractile material, particularly
IMCL.
4. Potential mechanisms for impaired muscle contractile function
in obesity
To date, the exact mechanisms underlying impaired skeletal muscle
contractile function in obesity are unknown. However, several pertur-
bations in muscle structure including increased lipid deposition within
L.M. Bollinger
and between muscle fibers, decreased expression of non-contractile
proteins, and altered myosin heavy chain isoform expression, have been
identified which may play a role in impaired muscle strength and power
in obesity. Fig. 1 depicts a mechanistic basis by which these perturba-
tions may negatively affect skeletal muscle strength, power, and
endurance.
4.1. Lipid accumulation within skeletal muscle
Obesity is associated with increased lipid accumulation between
(intermuscular fat) and within (IMCL) skeletal muscle fibers. Excess
accumulation of intermuscular fat has been reported in computed
tomography (CT) scans of severely obese subjects and is seen as an
indicator of muscle quality [66,67]. Indeed, intermuscular fat is
approximately two to three times higher in obese compared to normal
weight older women [30,68]. Increased accumulation of intermuscular
fat is associated with decreased muscle strength [69,70] and impaired
physical function [70,71] in older adults. Maly et al. [70] demonstrated
that intermuscular fat is correlated (R = 0.36, p < 0.002) with
increased time to complete five consecutive sit-to-stand cycles. Further-
more, these authors showed that intermuscular fat accumulation was
approximately 20% greater in those with knee OA than healthy controls
[70]. Choi et al. [30] demonstrated that ultrasound echo intensity of the
quadriceps muscles, a surrogate of intermuscular fat infiltration, was
inversely related to skeletal muscle strength suggesting that decreased
muscle quality due to fat infiltration between muscle fibers impairs
force production.
IMCL accumulation in skeletal muscle of the obese is positively
associated with single fiber CSA (R = 0.342–0.529), and negatively
associated with maximal shortening velocity (R = −0.75) and specific
power (R = −0.69), but not specific force [30]. These data suggest
that, IMCL accumulation may contribute, in part, to increased muscle
CSA and decreased power production in obesity. Using a computer
simulation, Rahemi et al. modeled the effects of increasing fat content
of skeletal muscle and found that both absolute and specific force of
muscle fibers decreased linearly with increasing IMCL content.
4.2. Altered expression of sarcomeric proteins
In addition to increased lipid accumulation, obesity alters expres-
sion of both contractile and non-contractile sarcomeric proteins which
may affect muscle contractile properties at a cellular level. Obesity
alters the expression of cytoskeletal proteins which are major determi-
nants sarcomeric architecture. Using a mass spectrometry approach,
Hwang et al. [72] evaluated protein expression of over 1200 individual
skeletal muscle proteins in lean and obese volunteers. Interestingly,
these researchers found that protein expression of α-actinin 2 and
desmin were significantly decreased in skeletal muscle of obese donors.
It is well established that α-actinin 2 is essential for anchoring actin
filaments to the z-disk. Furthermore, desmin is known to be crucial for
muscle force production [73,74]. Therefore, it is possible that decreased
expression of these proteins contributes to decreased relative force
production in skeletal muscle of the obese. To date, the effects of
decreased expression of α-actinin 2 and desmin in obesity on biome-
chanics of individual sarcomeres, whole skeletal muscle, and whole
body movements are unknown.
In addition to cytoskeletal proteins, obesity alters expression of
sarcomeric contractile proteins, most notably, myosin heavy chain
[75–78]. Tanner et al. [75] noted that percentage of type IIb myosin
heavy chain fibers (25.1 vs. 14.4%) was significantly higher and the
proportion of type I myosin heavy chain fibers (41.5 vs. 54.6%) was
significantly lower in obese vs. lean women. Indeed, these authors
reported that the relative proportion of type IIb myosin heavy chain
increased linearly (r = 0.48) with increasing BMI. It is well established
that physical inactivity [79], muscle unloading [80], and spinal cord
isolation [81] reduce the expression of type I MHC and increase
105
Gait & Posture 56 (2017) 100–107
expression of type IIx MHC. Conversely, aerobic [82] or resistance
[83] exercise training appear to increase in the proportion of fibers
containing type I MHC and decrease the proportion of fibers containing
type II MHC. Therefore, it is difficult to distinguish the effects of obesity
and physical inactivity on MCH isoform expression in obese humans.
Interestingly, Bollinger et al. [78] reported that protein expression of
type I myosin heavy chain was decreased in cultured human skeletal
muscle (HSkM) myotubes from extremely obese women. Since these
myotubes are cultured in similar conditions in vitro for several
passages, these data suggest that altered myosin heavy chain expression
in obesity may be, in part, due to a genetic or epigenetic effect and may
not respond to weight loss or exercise intervention. Indeed, Kern et al.
[84] noted that diet induced weight loss had no effect on myosin heavy
chain isoform expression in obese subjects. It is unclear whether
exercise interventions significantly alter skeletal muscle fiber type in
obesity. Therefore, it is apparent that obesity induces a slow-to-fast
fiber type shift which may contribute to premature volitional fatigue in
obesity [26].
5. Effects of obesity on skeletal muscle recruitment
Skeletal muscle recruitment patterns may also explain some of the
contractile dysfunction seen in obesity. EMG activity of the quadriceps
and gastrocnemius during gait is increased in obesity [34] suggesting
that motor unit recruitment may be altered in obesity. Increased muscle
activation in obesity may be due to a simple overload stimulus of excess
adipose tissue during ADLs. Indeed, load carriage studies have shown
that even moderate increases (15%) in body mass are sufficient to
increase EMG activity of the gluteus maximus (26%) and rectus femoris
(46%) during sit-to-stand [85]. External loads of 45% of total body
mass further increases activity of these muscles (approximately 200%)
and increases activity of biceps femoris (65%), vastus medialis (55%),
and medial gastrocnemius (43%) [85]. However, it is less clear how
obesity affects the ability to recruit skeletal muscle fibers at a
neuromuscular level.
Using an interpolated twitch response, Blimkie et al. [35] reported
that voluntary quadriceps motor unit activation (85.1 v. 95.3%) was
decreased in obese adolescent males during knee extension exercise. In
agreement with this, Tomlinson et al. [27] reported that voluntary
plantar flexor activation (interpolated twitch) was significantly lower in
young women with high body fat percentage (> 40%) compared to
their lean peers. However, this effect was not seen in older adults.
It should be noted that simultaneous recruitment (co-activation) of
agonist and antagonist muscles may contribute to decreased muscle
strength and power in obesity. However, few studies have examine
skeletal muscle co-activation in obesity. It has previously been reported
that tibialis anterior activation during maximal isometric plantarflexion
is unaffected by body mass [27], suggesting that decreased agonist
activation, but not increased co-activation of antagonists, may con-
tribute to decreased relative muscle strength and power and premature
volitional fatigue in obesity. It is possible that decreased agonist muscle
recruitment could contribute to relative skeletal muscle weakness and
decreased power in obesity.
6. Conclusions
Obesity alters whole body kinematics and joint kinetics which may
increase risk of musculoskeletal injury, development of osteoarthritis,
and physical disabilities. Although weight loss interventions have
shown promise to reduce the biomechanical effects of obesity, these
are typically only moderately successful (approx. 10% body mass
reduction) and are typically accompanied by subsequent weight regain.
Therefore, it is important to determine the role of other factors, in
biomechanics.
Clearly, obesity induces numerous alterations within skeletal muscle
ultimately resulting in decreased relative strength, decreased relative
L.M. Bollinger
Fig. 2. Potential influence of skeletal muscle contractile dysfunction on biomechanics in obesity. Obesity-induced alterations in biomechanics have largely been attributed to excess body
mass. The exact role of muscle contractile dysfunction in altered movement patterns, functional limitations, and increased risk of joint injury and/or disease remains unknown.
power, and premature volitional fatigue. However, the mechanisms
underlying these adaptations and their ultimate effect on bodily move-
ments and joint loading remains unexplored. We present Fig. 2 as a
conceptual model to demonstrate potential effects of skeletal muscle
contractile dysfunction on whole body biomechanics. We postulate that
skeletal muscle contractile dysfunction contributes, in part, to altered
movement patterns by increasing reliance on synergist muscles and
altering muscle recruitment patterns. We further hypothesize that
muscle contractile dysfunction contributes to development of func-
tional limitations by increasing the relative intensity (% MVIC) and
decreasing speed of ADLs and reducing participation in daily physical
activity. Finally, we hypothesize that muscle contractile dysfunction
may play a role in joint injury and disease susceptibility by decreasing
joint stability and increasing joint loading during ADLs. Future research
should aim to uncover the role of skeletal muscle dysfunction in
obesity-induced biomechanical alterations. Additionally, future re-
search should be aimed at determining how improving skeletal muscle
contractile function affects biomechanics in obesity. It is possible that
increasing skeletal muscle contractile function, independent of changes
in body mass, may mitigate some of the negative effects of obesity on
whole-body kinematics and joint kinetics.
Conflict of interest statement
The author declares no conflicts of interest.
Funding
N/A.
Acknowledgement
None.
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