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The biomechanical mechanism of how strength


and power training improves walking speed in
old adults remains unknown

Article in Ageing research reviews · March 2013


Impact Factor: 4.94 · DOI: 10.1016/j.arr.2013.03.001 · Source: PubMed

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Chantal Beijersbergen Urs Granacher


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Ageing Research Reviews 12 (2013) 618–627

Contents lists available at SciVerse ScienceDirect

Ageing Research Reviews


journal homepage: www.elsevier.com/locate/arr

Review

The biomechanical mechanism of how strength and power training


improves walking speed in old adults remains unknown
C.M.I. Beijersbergen a , U. Granacher b , A.A. Vandervoort c , P. DeVita d , T. Hortobágyi a,∗
a
University Medical Center Groningen, Center for Human Movement Sciences, Groningen, The Netherlands
b
University of Potsdam, Department of Training and Movement Sciences, Potsdam, Germany
c
The University of Western Ontario, Faculty of Health Sciences, School of Kinesiology, Canadian Centre for Activity and Aging, Canada
d
East Carolina University, Department of Kinesiology, Greenville, NC, USA

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

Article history: Maintaining and increasing walking speed in old age is clinically important because this activity of daily
Received 9 January 2013 living predicts functional and clinical state. We reviewed evidence for the biomechanical mechanisms of
Received in revised form 4 March 2013 how strength and power training increase gait speed in old adults. A systematic search yielded only four
Accepted 7 March 2013
studies that reported changes in selected gait biomechanical variables after an intervention. A secondary
Available online 15 March 2013
analysis of 20 studies revealed an association of r2 = 0.21 between the 22% and 12% increase, respectively,
in quadriceps strength and gait velocity in 815 individuals age 72. In 6 studies, there was a correlation of
Keywords:
r2 = 0.16 between the 19% and 9% gains in plantarflexion strength and gait speed in 240 old volunteers age
Aging
Strength training 75. In 8 studies, there was zero association between the 35% and 13% gains in leg mechanical power and
Power training gait speed in 150 old adults age 73. To increase the efficacy of intervention studies designed to improve
Gait biomechanics gait speed and other critical mobility functions in old adults, there is a need for a paradigm shift from
conventional (clinical) outcome assessments to more sophisticated biomechanical analyses that examine
joint kinematics, kinetics, energetics, muscle-tendon function, and musculoskeletal modeling before and
after interventions.
© 2013 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619
2. Age-related mechanical plasticity of gait: a distal-to-proximal shift in muscle function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619
2.1. Walking kinematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619
2.2. Effects of age on hip joint function during gait . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 620
2.3. Effects of age on knee joint function during gait . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 620
2.4. Effects of age on ankle joint function during gait . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 620
3. Scant biomechanical evidence for how strength interventions increase gait speed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
3.1. Search toward effects of specific strength and power training on gait characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
3.2. Selection criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
3.3. Quality assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
4. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 622
4.1. Quality assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 622
4.2. Evaluation of the four intervention studies identified by the systematic search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 622
4.3. Association between improvements in gait speed and muscle strength and power . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 622
5. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 623
5.1. The role of relative effort . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 623
5.2. Biomechanical mechanisms of interventions increasing gait speed in old adults . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 624

∗ Corresponding author at: Center for Human Movement Sciences, University Medical Center Groningen, A. Deusinglaan 1, Room 334, Building 3215,
9700 AD Groningen, The Netherlands. Tel.: +31 50 363 2645; fax: +31 50 363 3150.
E-mail address: t.hortobagyi@umcg.nl (T. Hortobágyi).

1568-1637/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.arr.2013.03.001
C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627 619

6. Summary and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 625


Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 626
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 626
Appendix A. Supplementary data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 626
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 626

1. Introduction capacity become incorporated into the movements of ADLs and in


case of gait, produces longer steps and faster walking. Although a
Aging, whether along healthy or non-healthy paths, modifies handful of studies did examine how specific interventions affect
human gait. While aging after age 50 modifies many gait char- selected biomechanical variables in relation to gait speed, no stud-
acteristics, shorter steps and slower walking speed may be the ies to date have reported the association between improvements
most functionally meaningful. The magnitude of the reductions in in maximal voluntary strength and power and the improvements
step length and walking speed are associated with the magnitude in lower extremity joint kinetics and energetics, identifying the
of any decline in health while aging. Consequently, self-selected mechanisms behind intervention-induced improvements in gait
habitual gait speed measured on a level surface is a marker and speed. The aim of the present review was to draw attention to a
predictor of many clinical conditions, including daily function, critical gap in our understanding as to how interventions improve
late-life mobility, independence, falls, fear of falls, fractures, mental mobility functions in old adults in general and, in particular, how
health, cognitive function, adverse clinical events, hospitalization, strength and power training improve gait speed in old adults. We
institutionalization, and survival (Abellan van Kan et al., 2009; addressed the question, ‘What is the biomechanical mechanism of
Atkinson et al., 2007; Dargent-Molina et al., 1996; Granacher interventions increasing gait speed in old adults?’ First we review
et al., 2011a; Guralnik et al., 2000; Ijmker and Lamoth, 2012; the age-related reorganization of mechanical output at the hip,
Potter et al., 1995; Studenski et al., 2011; Viccaro et al., 2011; knee, and ankle joints during gait and link these torques to the
Watson et al., 2010; Weuve et al., 2004). Gait speed in old adults, maximal torque available in the lower extremity joints. Finally, we
i.e., age over 70, that is similar to young adults’ speed signifies review the effects of strength interventions on gait biomechanics,
multi-systemic wellbeing and slowed gait suggests clinical or summarize the potential mechanisms, and make recommendations
sub-clinical impairments (Abellan van Kan et al., 2012). for future research.
Usual gait speed decreases up to 16% per decade starting already
at age 60 (Abellan van Kan et al., 2009, 2012; Bassey et al., 1982; 2. Age-related mechanical plasticity of gait: a
Bendall et al., 1989; Himann et al., 1988). Many old adults’ usual gait distal-to-proximal shift in muscle function
speed decreases to the functionally inadequate levels of 0.8 m/s and
even slower (Abellan van Kan et al., 2009), signifying mobility dis- 2.1. Walking kinematics
ability. The slowing of gait perpetuates physical inactivity because
the time needed to cross the street or reach a destination becomes Healthy aging after age 50 produces profound modifications in
too long and old adults lose motivation to ambulate (Bollard and gait. Step length, step rate and their product, walking velocity, are
Fleming, 2012). Step length shortens and gait speed slows due to fundamental sagittal plane biomechanical descriptors of walking.
sarcopenia, dynapenia, reduced joint range of motion, weakness, Self-selected walking velocity is lower in old (∼1.15 m/s) com-
fatigue, and lower dynamic stability (Abellan van Kan et al., 2012; pared with young (∼1.32 m/s) adults (Himann et al., 1988; Judge
Clark and Manini, 2012; Manini and Clark, 2012; Mitchell et al., et al., 1996; Kerrigan et al., 1998; Ko et al., 2009; McGibbon and
2012). Additional reasons for short step length and reduced gait Krebs, 2004; Schimpl et al., 2011). This decline in walking velocity
speed are the desire to walk with a greater sense of stability and is associated with reduced step length (Hageman and Blanke, 1986;
the strategy to avoid high forces causing joint pain (Abellan van Kerrigan et al., 1998, 2001; Ko et al., 2009; McGibbon and Krebs,
Kan et al., 2009). Maintaining usual gait speed in old age is of major 2004; Ostrosky et al., 1994; Winter et al., 1990) and increased step
clinical and functional significance as it is clear that old individuals rate or cadence (Judge et al., 1996). The increase in cadence however
with faster usual and maximal gait speeds have greater longevity is not sufficient to offset the decrease in step length, thereby reduc-
(Abellan van Kan et al., 2009; Studenski et al., 2011; Ostir et al., ing velocity. Furthermore and as a consequence of reduced step
2007). Further, although as yet not directly proven, these cross- length, double support time increases with concomitant reductions
sectional studies support the attractive hypothesis that increasing in single support and swing times (Begg and Sparrow, 2006; DeVita
step length and gait speed may even increase longevity. and Hortobágyi, 2000). It is thought that these latter adaptations
Unsurprisingly there is a massive ongoing preventative effort increase dynamic stability in the elderly (DeVita and Hortobágyi,
to improve old adults’ abilities to successfully perform activities of 2000). Whereas more recent studies suggest that another strategy
daily living (ADLs) (e.g., (Fielding et al., 2011). Within this effort a to improve stability with aging is a wider support base or step width
clear target is to slow the rate of gait speed loss in healthy old adults (Dean et al., 2007). Overall, it is well documented that basic gait
and to restore gait speed in those patients who suffer from mobility kinematics, including walking velocity and its related factors, are
disability and such other clinical conditions as cancer, neuropathy, changing with age.
and osteoarthritis. Numerous interventions, applying resistance, Locomotion biomechanics have been compared between young
power, balance, and specific locomotor training have demonstrated and old adults while walking at both identical and different,
remarkable increases in maximal voluntary muscle strength and self-selected walking velocities. Both comparisons are important
power up to 85% and as much as 53% in gait speed (Granacher and identify different aspects about locomotion biomechanics in
et al., 2011a; Mian et al., 2007a). The common element of the old adults. Self-selected velocities are more ecologically sound and
intervention studies that provides the pretext for this review is a identify behaviorally meaningful age-related differences in gait.
complete absence of addressing the mechanisms of how interven- The slower walking speed typically selected by old adults manifests
tions increase gait speed in old adults. Although clinicians routinely itself in lower joint torques and powers and these directly produce
prescribe interventions for old adults (Fielding et al., 2011), we do shorter steps and lower velocity (DeVita and Hortobágyi, 2000).
not know how, if at all, does the intervention-improved physical Due to the shorter steps, old adults also produce less work per step
620 C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627

(Winter et al., 1990). Matched velocity comparisons on the other Additional studies are needed to resolve these clinically critical
hand have value because these show neuromuscular adaptations inconsistencies in knee function during gait.
strictly due to aging physiology without the confounding effects
of age and velocity. We note that while horizontal velocities are
2.4. Effects of age on ankle joint function during gait
often monitored or controlled in these studies, vertical kinematics
are typically completely unmonitored and unconstrained (but see
In contrast to the findings on knee biomechanics, mechanical
(Persch et al., 2009). Differences in vertical displacement profiles
changes at the ankle joint during walking and due to age are highly
between young and old, for example, would be a direct outcome of
consistent within the literature (McGibbon, 2003). Old vs. young
differences in muscle work and would be associated with different
adults maintain their position of the foot closer to the anatomical
metabolic and mechanical costs of walking. While the observed
position during stance phase and they show less range of motion in
age-related gait differences such as the increased metabolic cost
the gait cycle (DeVita and Hortobágyi, 2000). Many studies reported
of walking in old adults may be related to altered neural activation
old adults to walk with a reduced plantarflexion peak position just
during gait (Hortobagyi et al., 2011; Peterson and Martin, 2010), it
before push-off (Cofre et al., 2011; DeVita and Hortobágyi, 2000;
is possible that such differences are also due to vertical kinematics
Kerrigan et al., 1998; Monaco et al., 2009; Silder et al., 2008) and also
(Dean et al., 2007; Mian et al., 2007a).
with a reduced plantarflexion torque during late stance (DeVita and
Hortobágyi, 2000) compared with young. Furthermore, it is clearly
2.2. Effects of age on hip joint function during gait
reported that healthy old adults have reduced ankle plantarflexor
power output during push-off compared with their younger coun-
Comparisons made at both identical and different velocities
terparts when gait speeds are matched (Cofre et al., 2011; DeVita
have shown significant changes with age in joint kinematics and
and Hortobágyi, 2000; Monaco et al., 2009). Ankle power genera-
kinetics at the hip, knee and ankle joints. Old compared with young
tion during push-off plays an important role in forward progression
adults show greater range of motion at the hip throughout each
of the body, and consequently the reduction in stride length and
gait cycle (Cofre et al., 2011; DeVita and Hortobágyi, 2000; Silder
increased double leg support that occur with increasing age can be
et al., 2008). Along with greater hip range of motion, old adults
at least partially attributed to the reduction in power production of
walk with larger internal hip extensor torque and positive power
the calf muscles.
in early stance phase and more internal hip flexor torque and posi-
Overall old adults use lower plantarflexor torque and generate
tive power during late stance compared with young adults (DeVita
less positive ankle power during push-off and there is a concur-
and Hortobágyi, 2000). The duration of the hip extensor torque
rent increase in peak hip extension power during early stance
and power generation was also longer in old compared to young
and peak hip flexor power generation during late stance. Fig. 1
adults, producing larger total angular impulse and work at the
shows this “redistribution of joint powers” and the overall dis-
hip (DeVita and Hortobágyi, 2000). Overall, old adults increase hip
tal to proximal shift in muscle function, a phenomenon coined as
range of motion, torque, power and work during walking compared
the age-related mechanical plasticity of human gait (DeVita and
to young adults when gait velocity is matched. In fact, it appears
Hortobágyi, 2000). Numerically, there was an 19% reduction in
that a wider step width (i.e., more dynamic stability) is associated
mass-normalized ankle power and 38% increase in hip power as
with increased hip muscle activity without concurrent changes
healthy volunteers walked at a range of speeds between 1.0 and
in the activation of ankle evertors and invertors (Winter, 1995).
1.5 m/s in 8 studies (Cofre et al., 2011; DeVita and Hortobágyi, 2000;
Further, increased hip joint function with age was also important
Judge et al., 1996; Kerrigan et al., 1998; McGibbon and Krebs, 2004;
for increasing walking velocity. Old adults increased their walking
Monaco et al., 2009; Savelberg et al., 2007; Silder et al., 2008) (Table
velocity from comfortable to fast pace by increasing the internal
S1, online supplement).
hip extensor torque and positive power in early stance or their hip
flexion torque and positive power in late stance (Graf et al., 2005;
Judge et al., 1996; Kerrigan et al., 1998).

2.3. Effects of age on knee joint function during gait

Gait changes at the knee showed greater knee flexion during


initial contact but less knee flexion in early stance for old com-
pared with young adults (DeVita and Hortobágyi, 2000). Reduced
flexion in early stance was the primary kinematic adaptation pro-
ducing the more erect walking pattern with a lower knee extensor
torque seen in old adults. Adaptations in knee torque as a con-
sequence of age are inconsistent: knee extensor angular impulse
during early stance, representing knee extensor torque, was lower
in one (DeVita and Hortobágyi, 2000) but similar in another study
(McGibbon and Krebs, 2004). In fact, when normalized to mass
and height, old adults walked with greater knee extensor torque
and concomitant negative work and negative peak powers dur-
ing loading response (Monaco et al., 2009). Based on their mean
mass and height values their non-normalized data would appear to
show even larger torque and power for old adults compared with
young. These discrepancies in knee torque results led to additional
contradictory results in knee joint power because there was less Fig. 1. Mechanical plasticity of old adults’ gait. Body mass normalized hip, knee,
positive and negative work, and therefore less power output at the and ankle power during stance phase of gait, showing a 38% shift in function to hip
extensors concomitant with an 19% reduction in ankle plantarflexor power in old
knee in one case (DeVita and Hortobágyi, 2000), whereas others
adults during the stance phase of gait. Joint powers were recorded under 6 walking
reported greater power output for old compared with young adults conditions ranging in walking speed between 1.0 and 1.5 m/s in 7 studies. * p = 0.050
(Cofre et al., 2011; McGibbon and Krebs, 2004; Monaco et al., 2009). at hip and p = 0.022 at ankle between young and old adults.
C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627 621

Fig. 2. Flowchart describing the systematic search.

In summary, these data illustrate that there are multi-focal age- literature search up to November 2012 using the following terms
related adaptations in gait kinematics and kinetics. Next we review in the MEDLINE and COCHRANE search: (“aged [MeSH]”) AND
the evidence for strength interventions causing adaptations in gait (“gait [MeSH]” OR “locomotion [MeSH]” OR “walking [MeSH]” OR
biomechanics and increases in old adults’ gait speed. “ambulation [Text Word]”) AND (“exercise [MeSH]” OR “resistance
training [MeSH]” OR “power training [Text Word]”) AND “biome-
3. Scant biomechanical evidence for how strength chanics [MeSH]” OR “kinetics [MeSH]” OR “power [Text Word]” OR
interventions increase gait speed “joint [Text Word]”. The search was limited to English language
and age ≥65. Duplicates appearing in both searches were removed.
Based on 55 studies, a previous review analyzed the effects Fig. 2 summarizes the searches.
of exercise interventions on locomotor function in old adults
(Mian et al., 2007a). The nature of interventions varied widely and 3.2. Selection criteria
included strength, power, balance, flexibility, aerobic, and mobility
exercise protocols or combinations thereof. Most studies used self- Studies were included in the review if: (a) study participants
selected gait velocity as a primary outcome to quantify the effects were aged ≥65 years; (b) performed strength or power intervention
of an intervention along with performance-oriented tests such (except otherwise stated due to a limited number of studies avail-
as fast walking velocity, stair climbing velocity, 6-min walk dis- able), and (c) if a study incorporated at least one gait biomechanical
tance, and up-and-go test time. As expected, self-selected velocity outcome measure. Studies were excluded if: (a) participants had a
increased 14% and the time to perform the walking tests decreased history of neurological disease, (b) participants were amputees or
12%, suggesting that old adults adapt and benefit from exercise used prosthesis; or (c) they were not written in English. Based on
therapy through improvements in spatio-temporal gait character- these criteria, we analyzed the abstracts of any potentially rele-
istics (Mian et al., 2007a). However, the review also highlighted vant papers and performed accordingly content analysis of the full
the remarkable omission in the literature as to how little we know paper.
about the biomechanical mediators of increased walking velocity
associated with exercise interventions, a mechanism that remains 3.3. Quality assessment
unknown today.
Two reviewers assessed the methodological quality of the
3.1. Search toward effects of specific strength and power training included studies using the Physiotherapy Evidence Database
on gait characteristics (PEDro) scale. The PEDro scale rates randomized controlled trials
from 0 to 10 with a score above 6 representing high quality (Maher
To address the issue of biomechanical mediators and extend the et al., 2003).
previous review (Mian et al., 2007a), we conducted a systematic
622 C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627

4. Results The authors did not compute or report the association between
changes in strength and gait kinematics and kinetics.
The flow chart in Fig. 2 summarizes the systematic review. The Cao et al. showed that a 12-week-long intervention consisting
search identified 724 studies (MEDLINE n = 669; COCHRANE n = 55). of aerobic, balance, strength, coordination, and walking exercises
After the elimination of 30 duplicates and 675 studies based on did not improve step length and gait velocity. However, old adults’
title or abstract, additional 15 studies were eliminated based on gait became more dynamic as they walked with more hip flexion at
eligibility criteria. In the end, four studies met the inclusion criteria heel-contact and toe-off in the stance and through the swing phase
and were retained for analysis. (Cao et al., 2007). Further, there was more knee flexion at heel-
contact and during swing-phase and more ankle plantarflexion at
4.1. Quality assessment toe-off. The dynamic range of motion at the ankle increased 3.7◦
(p < 0.05). Even though the authors used the 30-s chair stand test
The mean quality score for the 4 included studies was 5.5 ± 2.4 to indirectly measure leg strength, they attributed the changes in
(range, 2–7). We included a single arm study without a control gait kinematics to improvements in ankle strength. The authors did
group, scoring only 2. The other three studies had a PEDro score not compute or report the association between changes in strength
between 6 and 7, suggestive of high quality (Persch et al., 2009; and gait kinematics.
Hartmann et al., 2009; McGibbon et al., 2003).
4.3. Association between improvements in gait speed and muscle
4.2. Evaluation of the four intervention studies identified by the strength and power
systematic search
Based on an extensive search and analysis of the literature,
Hartmann et al. examined the effects of a 12-week strength we found limited biomechanical evidence to explain how inter-
training program with and without foot gymnastics on muscle ventions in general and strength and power training in particular
strength and gait kinematics measured with a trunk accelerometer improve walking speed in old adults. Current evidence is insuffi-
in healthy old adults age 76 (Hartmann et al., 2009). Knee and ankle cient and inconsistent to explain how and if at all newly acquired
strength increased 14–46% (p < 0.05) and gait parameters improved strength and power become incorporated in the locomotor muscles
1–11%, with gait speed and step length improving similarly 6.6% that drive the limbs during gait. In lieu of kinematic and kinetic gait
and 5.0% in the two groups (p < 0.05). The training program supple- data, we argue that the next best available evidence to determine if
mented with foot gymnastics increased ankle range of motion to improved muscle strength is a moderator of increase in gait speed
11.9◦ from 11.1◦ (p = 0.036). The authors did not compute or report is to quantify the association between improvements in gait speed
the association between changes in strength and gait kinematics. and gains in muscle strength and power.
Persch et al. observed that 12 weeks of strength training We were able identify 4 studies that reported such correla-
improved maximal isometric strength of the hip, knee, and ankle tions. Judge et al. reported r2 = 0.31 (p > 0.05) association between
muscles 60% and also increased step length (0.14 m), gait speed leg strength and gait speed in 31 community-dwelling adults age
(0.13 m/s), and cadence (11 steps/min) (all p < 0.05) in healthy 82 before a strength training intervention and stated that this
adults age 61 (Persch et al., 2009). After strength training, sub- association did not change after the intervention, suggesting no
jects struck the ground with 3.7◦ , 2.6◦ , and 1.1◦ more peak hip, independent role for muscle strength in improving gait speed
knee, and ankle flexion and walked with 5.6◦ , 0.8◦ , and 4.0◦ more (Judge et al., 1993). Persch et al. observed an association of r2 = 0.44
hip, knee, and ankle range of motion in the stance phase (all (p = 0.001) and r2 = 0.17 (p = 0.049) between changes in knee exten-
p < 0.05). Despite the larger flexion in the lower extremity joints, sor and hip flexor strength, respectively, and stride length (thus
somewhat paradoxically, the vertical displacement of the center of indirectly with gait speed) in 14 old adults age 61 (Persch et al.,
mass decreased 8 mm (p < 0.01), suggesting a less dynamic albeit 2009). Hruda et al. reported r2 = 0.22 and r2 = 0.18 (both p < 0.05)
faster gait. Changes in plantarflexor strength were associated with between changes in leg extensor power and, respectively, changes
changed in cadence r2 = 0.30 (p < 0.05) but not with changes in gait in 8-ft up-and-go and 6-minute walk time in 18 healthy old adults
speed. Changes in knee extensor strength correlated with changes age 85 (Hruda et al., 2003). Granacher et al. found a non-significant
in stride length r2 = 0.44 (p < 0.05) and changes in hip flexor strength association of r2 = 0.04 between changes in plantarflexor strength
correlated with changes in stride length r2 = 0.17 (p < 0.05). Thus, and gait velocity as a result of an 8-week-long strength and bal-
improved knee extensor function through training plays a relatively ance intervention performed in 17 healthy adults age 56 (Granacher
more important role in improving gait speed than changes in ankle et al., 2011b). Overall, improvements in leg strength accounted for
and hip flexor function. 23% of the variation in old adults’ improved gait speed.
McGibbon et al. compared the effects of 6 weeks of strength To pinpoint the role of individual muscles, we identified 20 stud-
or functional training in small samples of old adults age 75, ies and extracted data for changes in maximal voluntary quadriceps
with at least one lower extremity impairment (McGibbon et al., strength and gait velocity. The twenty studies represent a total of
2003). Functional training improved leg strength (26%) significantly 815 subjects with a mean age of 72, which we think fully captures
more than strength training (16%). Functional training improved the relation between quadriceps strength and improvements in gait
gait velocity significantly (p = 0.001) more (0.178 m/s increase) speed in old adults. On the average, there were 30 subjects per study
than strength training (0.055 m/s increase). Ankle kinetics dur- who exercised for 18 weeks. Gait speed was assessed over an aver-
ing gait improved 56% in the functional training group and 9% age distance of 22 meter or timed over 5.5 min. Initial and final gait
in the strength-training group (difference p = 0.024) as measured speed was 1.25 (range 0.45–2.01) and 1.38 (0.49–2.35) m/s, a 12%
by ankle plantarflexor mechanical energy expenditure but only increase. Mean quadriceps strength was 134 (10–423) at baseline
the functional group improved knee kinetics 108% compared with and improved 22% to 171 (8–753) Nm after interventions. Based
27% decrease in the strength-training group (difference p = 0.038). on the data in these 20 studies, Fig. 2A shows an association of
Hip extensor mechanical energy expenditure decreased 10% after r2 = 0.21 (p < 0.018) between the changes in quadriceps torque and
functional but increased 97% after strength training (difference gait speed (Table S2, online supplement).
p = 0.053). Although improvements in gait were similar in the two Because the largest declines occur in plantarflexor compared
groups, the authors concluded that improved coordination of mus- with knee and hip joint powers during gait (Fig. 1), we identi-
cle power mediated the improved mobility in the functional group. fied studies that measured the changes in maximal plantarflexor
C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627 623

voluntary torque and gait speed before and after strength training.
In 6 such studies, representing 240 subjects with a mean age of 75,
participants exercised for 22 weeks. Gait speed was assessed over
21 m or 5.3 min. Initial and final gait speed was 1.21 (0.81–1.38)
and 1.30 (1.02–1.48) m/s, a 9% increase, and plantarflexor strength
was 79 (21–372) and 94 (25–383) Nm, 19% higher, after interven-
tion. Fig. 2B shows an association of r2 = 0.16 (p = 0.432) between
the changes in strength and gait speed in the 6 studies (Table S2,
online supplement).
Considering the increasing emphasis on power vs. strength
training to improve function and gait speed in old adults (Reid
and Fielding, 2012), we have identified 8 studies that measured
leg power and gait speed before and after power training, repre-
senting 150 subjects age 73. On the average, 17 subjects per study
exercised for 12 weeks. Gait speed was assessed over an average
distance of 5.7 m. Initial and final gait speed was 1.15 (0.54–1.26)
and 1.26 (0.78–1.99) m/s, a 13% improvement, and leg power was
170 (6–613) and 228 (7–803) W, signifying a 19% improvement.
Fig. 2C shows an association of r2 = 0.00 (r2 = 0.005 after the removal
of a value of near 50% change in gait speed, p = 0.990) between the
changes in leg power and gait speed in the 8 studies (Table S2,
online supplement).

5. Discussion

It is known that muscle strength in old adults is related to


ADL performance, including walking and that strength training
improves many physiological characteristics in old adults, resulting
in better mobility and higher walking speed (Chandler et al., 1998;
Granacher et al., 2011a; Judge et al., 1993). Yet we have identified
a key gap in our understanding as to how interventions improve
mobility function in general and how, in particular, strength and
power interventions improve gait speed in old age. In short, despite
these known associations, increases in muscle strength are poorly
correlated with increases in step length and gait velocity in old
adults. We discuss the role of relative effort in mechanical plastic-
ity of gait and candidate mechanisms of how strength interventions
improve gait speed.

5.1. The role of relative effort

When young and old adults walk at a speed of 1.5 m/s in a lab-
oratory, the mechanical power output of muscles supporting the
body and then driving the leg from stance to swing becomes reor-
ganized with age: the locus of function shifts to the proximal hip
Fig. 3. Associations between changes in gait speed and changes in leg strength or
muscles from the distal ankle muscles (Fig. 1). The reduction in
power based on studies in the literature. Panel A: Association between changes in
ankle muscle mechanical output can reach as much as 27% (DeVita maximal voluntary quadriceps knee extension torque and gait speed measured on
and Hortobágyi, 2000) with a 12% reduction still present even if old a level surface in 20 studies. There are 26 data points in the graph because a few
compared with young adults walk 13% faster (Kerrigan et al., 1998). studies reported multiple measures of muscle strength or gait speed. The associa-
tion is characterized by y = 063x + 14.3 and r2 = 0.21 (p < 0.018). Panel B: Association
Expressing leg mechanical output recorded during gait in rela-
between changes in maximal voluntary plantarflexor torque and changes in gait
tion to the maximal available effort allows us to operationalize speed measured on level surface in 6 studies. There are 12 data points in the graph
mechanical plasticity of gait. The idea is that the reduced ankle because several studies reported multiple measures of muscle strength or gait speed.
function seen in old adults’ gait is associated with a reduction in The association is characterized by y = 0.58x + 13.8 and r2 = 0.16 (p = 0.421). Panel C:
maximal voluntary torque generation. There is strong evidence for Association between changes in maximal voluntary leg power and changes in gait
speed measured on level surface in 8 studies. There are 9 data points in the graph
a preferential decline in structure and function of nerves and mus-
because 1 study reported multiple measures of leg power or gait speed. The associ-
cles of lower compared with upper extremity due to age (for a ation is characterized by y = 0.02x + 34.6 and r2 = 0.00 (p = 0.996). The removal of the
review see (DeVita and Hortobágyi, 2000). However, the reductions extreme value at the right does not affect the association. Table S2 lists the source
in hip and knee muscle strength compared with the ankle plan- data and references used to construct the graphs in panels A, B, and C.
tarflexors strength were similar in men age 75. In addition, ankle
plantarflexors compared with hip extensors were only 8% weaker
in women age 73 (Danneskiold-Samsoe et al., 2009). Therefore, the knee, and ankle joints as a percent of the maximal torque avail-
distal vs. proximal weakness within the lower extremity may be able at the same joints (cf. also (Hortobágyi et al., 2003). Because
less robust than the differences between upper and lower extrem- maximal torque loss is similar in hip, knee, and ankle extensors
ities. Still, using these limited data, Fig. 4 shows for the first time (Danneskiold-Samsoe et al., 2009), the torques generated during
the relative effort during gait, i.e., the level of effort used at the hip, gait are the primary determinants of relative effort. The relative
624 C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627

5.2. Biomechanical mechanisms of interventions increasing gait


speed in old adults

The most obvious mechanism of an intervention designed to


improve muscle strength and gait speed is that the newly acquired
muscle strength and power increases joint torques and powers that
support the leg in stance phase, provides the energy for the push off,
and drives the limb into swing. Fig. 5 provides one model that con-
siders a successful incorporation of newly acquired strength into
gait (Fig. 5A) and shows another model that predicts an increase in
gait speed with little or no incorporation of newly acquired muscle

Fig. 4. Relative effort during gait in young and old adults, computed as the percent
of mechanical output measured during gait relative to the maximal voluntary torque
measured on an isokinetic dynamometer at 30◦ /s (hip, knee) and 15◦ /s (ankle). The
gait data are based on 7 studies presented also in Fig. 1. The isokinetic torque data are
based on the only study to date that report maximal hip, knee, and ankle voluntary
torques within the same person (Danneskiold-Samsoe et al., 2009). Please refer to
the text for further interpretation of these data.

effort is the highest at the ankle; the above-maximal level is prob-


ably caused by the differences in joint positions where the peak
torques occur during gait and the isokinetic tests, the differences in
contraction velocities in the two conditions and by the differences
in subject characteristics between the 7 gait studies (Cofre et al.,
2011; DeVita and Hortobágyi, 2000; Judge et al., 1996; Kerrigan
et al., 1998; McGibbon and Krebs, 2004; Monaco et al., 2009;
Silder et al., 2008) and the one study reporting the isokinetic data
(Danneskiold-Samsoe et al., 2009). Nonetheless, the data suggest
that old adults walk near the maximal capacity of the ankle joint,
presumably causing ineffective push-off, shorter steps, and slower
gait. Apparently, the 35% increase in hip power is insufficient to
compensate for the reduction in ankle function and walking speed
decreases in old adults (DeVita and Hortobágyi, 2000). Mechani-
cal plasticity predicts that improving maximal voluntary strength
of the hip and knee muscles may have little impact on gait speed
because relative effort is low in these joints. In contrast, improving
maximal capacity of ankle plantarflexors may have a large impact
on gait (speed) as long as there is an enabling mechanism that
allows the use of the newly acquired strength.
The high relative effort at the ankle suggests that interventions
should focus on improving plantarflexion function. The expec-
tation is that the ankle torques and concomitantly gait velocity
would increase. This expectation assumes that old adults possess
an enabling mechanism that moderates the use of the newly
acquired strength into function. However, the results of this review Fig. 5. Conceptual models of how strength and power training interventions
provide virtually no evidence for either element of this expecta- improve gait speed in old adults. A: Old adults walked (filled column) just below
their maximal ability (open column) pre-training. The narrow difference between
tion. First, about 80% of interventions explicitly target the knee
the filled and open columns suggests a high relative effort during gait. Training
extensors even though, as this review has uncovered it (Fig. 1), increased maximum ability and adults now walk with more force than they pre-
the age-related changes in knee kinetics are minimal vis-à-vis the viously had yet with lower effort relative to their maximal ability. Maximal ability
20–40% reductions in maximal voluntary knee extension torque (open column) is quantified by joint torques measured through inverse dynamics
(Danneskiold-Samsoe et al., 2009; Hortobágyi et al., 1995). As of analysis in a test exercise such as a maximal leg press. In this model, old adults
are able to incorporate newly acquired muscle strength as shown by the increased
now, no interventions have specifically targeted the ankle plan- filled column in post- compared to pre-test. There is currently no evidence for the
tarflexors, which operate at the highest relative effort (Fig. 1), and incorporation model. B: Similar to the Model in A, old adults walked (filled column)
linked such changes in strength to changes in ankle kinetics in the just below their maximal ability (open column) pre-training. The narrow difference
same subjects. Second, the overall consensus from the 34 stud- between the filled and open columns suggests a high relative effort during gait.
Training increased maximum ability and adults now walk with more force than they
ies included in our analysis is that strength and especially power
previously had but not much more force, denoted by the small difference between
gains are weakly or not at all associated with changes in gait speed the two filled columns pre- and post-training. That is, the relative effort decreased
(Fig. 3), joint kinematics, and kinetics. Although these interven- less in Model B than in Model A. However, the effort needed to walk (filled column in
tions improve neuromuscular function 25% and old adults walk 11% post-test) is still below the pre-training maximum (open column in pre-test). This
faster, the evidence is weak that old adults walk faster because they model predicts little incorporation of newly acquired strength into gait. There is
indirect biomechanical evidence for this model. Ultimately, either mechanism still
use the newly acquired physical abilities in gait (Tables S1-2, online must act through the final common pathway of higher muscle force generation that
supplements). increases kinetic energy and gait speed.
C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627 625

strength (Fig. 5B). To date, there is no gait kinetics data to verify the already existing physiological resources and not because the new
incorporation model (Fig. 5A). The little biomechanical data avail- levels of strength or power increases the mechanical output of the
able show an inconsistent picture. Kinematic analysis revealed a ankle, knee, and hip joint muscles. Interventions may also increase
key role for knee function (Persch et al., 2009), whereas mechani- gait speed by improving the coordination between pairs of agonist
cal energy expenditure analysis showed a decreased role for knee and antagonist muscles which in turn could reduce the metabolic
function in gait speed adaptations (McGibbon et al., 2003). Even cost of transport and the relative effort (Hortobagyi et al., 2011;
within the same study, the pattern of association between changes Thomas et al., 2007a,b) and through an optimization of irregular
in strength and function was inconsistent: improved plantarflex- and variable gait (Lamoth et al., 2011; Springer et al., 2006; Stergiou
ion and hip function (6◦ more flexion) was marginally associated and Decker, 2011). Perhaps the mechanism acts through improved
(r2 = 0.17, p = 0.049) with gait speed but changes in knee function psychological, “strength,” i.e., self-efficacy, less resistance to rotate
and gait speed correlated r2 = 0.44 (p = 0.001) (Persch et al., 2009). joints through the range of motion, or a motor unit effect in which
The 6◦ more hip flexion is in line with predictions by mechani- even if maximum strength is not increased, motor units are more
cal plasticity (i.e., a shift of function to hip from the ankle) but then readily activated. Recent theories suggest that exercise may indeed
these changes poorly correlated with gait speed. On the other hand, reduce the rate of falls through its beneficial effects on cognitive
mechanical plasticity predicts not much need for a change at the function in old adults (Liu-Ambrose et al., 2013). There are also
knee (due to its low relative effort), yet increases in quadriceps profound age-related changes in tendon properties, including a
strength correlated strongest with changes in gait speed (r2 = 0.44, reduction in stiffness that can be modified by exercise training
p = 0.001). This last piece of data provides perhaps the first still (Narici and Maganaris, 2006; Reeves et al., 2006). Still, each and any
somewhat unconvincing hint that old adults may be able to incor- of these mechanisms must act through the final common pathway
porate a small portion of the newly acquired voluntary strength of higher muscle force generation that increases kinetic energy and
into knee function and causing changes in gait speed. Puzzlingly, gait speed.
a composite exercise program improved muscle strength 14% and Finally, we note that virtually any type of intervention even
produced kinematic adaptations at the hip, knee, and ankle joints. those not designed explicitly to improve muscle strength and
However, the larger range of motions, and presumably accelera- power can increase gait speed. Walking speed increased follow-
tions, at these joints did not increase gait speed (4%, n.s.) (Cao et al., ing balance, endurance, functional (Krebs et al., 2007), combination
2007). Thus, an intervention can modify gait biomechanics without (Cao et al., 2007; Mian et al., 2007b), walking training with (Thomas
a putative increase in gait speed. et al., 2006) and without (Earles et al., 2001) body weight unloading,
Although conceptually and empirically functional performance, and Tai Chi exercise (Wolf et al., 2006) (for a review see (Granacher
including gait speed, is associated with leg power ∼r2 = 0.50 (Bean et al., 2011a; Mian et al., 2007a; Paterson et al., 2007). Any and all of
et al., 2004; Cuoco et al., 2004; Fielding et al., 2002; Reid and the interventions clinicians currently prescribe for old adults can
Fielding, 2012) and modeling studies show increased gait speed improve neuromuscular function and perhaps the increased gait
with increased muscle power (Liu et al., 2008; Neptune et al., 2008, speed is a secondary but valuable outcome as are improvements in
2009; Pandy and Andriacchi, 2010; Pandy et al., 2010), our find- balance and sit-to-stand. This generalized effects of interventions
ing that improvements in leg power had r2 = 0.00 association with may be related to the idea that functional improvements after an
improvements in gait speed was unexpected (Fig. 2C, Table S2). We intervention dot not scale to a dose–response relationship because
interpret these data to mean that mechanism of adaptation in gait the stimulus for increasing gait speed is different in magnitude and
speed in response to power training is unknown and not under- nature than the exercise dose that improves maximal voluntary
stood. An extensive analysis of adaptations to strength and power force and power (cf. (Mian et al., 2007a). That is, the stimulus to
training in a previous review (Granacher et al., 2011a) provides a increase gait speed is lower in magnitude than the stimulus for
perspective for our finding of this low association between changes strength gains so that training with high loads elicits a response
in gait speed and changes in leg power. The idea is that perhaps the at lower level activities. After training old adults become stronger
changes in gait speed and leg power association would become and operate at lower relative levels of their maximal capacities and
much stronger if future studies followed more closely the exercise thus more comfortable absolute levels.
specificity principle by having old adults exercise at low intensi-
ties (20–40% of maximum power) improving both gait speed and
leg power (Orr et al., 2006). However, the mechanism is very likely 6. Summary and recommendations
multi-factorial and interactive between biomechanical, physiolog-
ical, neurological and psychological factors. Clinicians routinely prescribe strength and power interventions
Anyone will increase walking speed by generating more mus- for old adults in an effort to improve ADL mobility, including
cle force and power but the current biomechanical data do not gait speed (Fielding et al., 2011; Reid and Fielding, 2012). The
bear out this mechanism. Fig. 5B describes a situation in which present review shows that the biomechanical mechanisms of how,
old adults operate close to maximum effort pre-training. Train- if at all, the intervention-improved physical capacity becomes
ing increases maximum effort and adults now walk with more incorporated into the movements of ADLs and in case of gait,
force than they previously had but not much more force and still produces faster walking, is not known. An analysis of over 30
below the pretraining maximum. Old adults operating closer to studies revealed that the association between improvements in
their performance limits (Hortobágyi et al., 2003) (Fig. 4) may leg muscle strength and gait speed is r2 = 0.21 and between the
not as well incorporate newly acquired maximal strength into changes in leg power and changes in gait speed is r2 = 0.00. To
locomotor tasks: they adopt strategies that allow them to use so far increase the efficacy of intervention studies designed to improve
unexploited resources more effectively. We speculate that perhaps gait speed and other critical mobility functions in old adults,
they use new and previously non-existent levels of muscle force there is a need for a paradigm shift from conventional outcome
and power. They may increase the use of force to levels that were assessments to more sophisticated biomechanical analyses that
already available before the intervention but for some reason were examine joint kinematics, kinetics, energetics, muscle–tendon
unused. In particular, it seems an equally reasonable and untested function, and musculoskeletal modeling before and after interven-
possibility that interventions improve gait speed because old adults tions. Physiological, neurological, and psychological tests could
simply feel more comfortable after the intervention as they operate enhance the biomechanical studies and identify the full spectrum
at a lower effort relative to their maximal capabilities and exploit of exercise-induced modifications in walking performance.
626 C.M.I. Beijersbergen et al. / Ageing Research Reviews 12 (2013) 618–627

We recommend that future studies perform whole body kine- Bollard, E., Fleming, H., 2012. A study to investigate the walking speed of elderly
matic and kinetic analyses of gait before and after strength and adults with relation to pedestrian crossings. Physiotherapy Theory and Practice.
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Conflict of interest Sciences and Medical Sciences 66, 1226–1237.
Graf, A., Judge, J.O., Ounpuu, S., Thelen, D.G., 2005. The effect of walking speed
None declared. on lower-extremity joint powers among elderly adults who exhibit low
physical performance. Archives of Physical Medicine and Rehabilitation 86,
2177–2183.
Acknowledgements Granacher, U., Meuhlbauer, T., Zahner, L., Gollhofer, A., Kressig, R.W., 2011a. Com-
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We thank Dr. Alessio Murgia, Professor Dr. Bert Otten, and Dr. Granacher, U., Wick, C., Rueck, N., Esposito, C., Roth, R., Zahner, L., 2011b. Promoting
Azusa Uematsu for their insightful comments. balance and strength in the middle-aged workforce. International Journal of
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subsequent disability: consistency across studies, predictive models, and value
of gait speed alone compared with the short physical performance battery.
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the online version, at http://dx.doi.org/10.1016/j.arr.2013.03.001. M221–M231.
Hageman, P.A., Blanke, D.J., 1986. Comparison of gait of young women and elderly
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