BJMB
Brazilian Journal of Motor Behavior
Special issue:
Effects of aging on locomotor patterns
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Editorial: Effects of aging on locomotor patterns
Paulo C. R. Santos
1,2
| Diego Orcioli-Silva
3
1
Department of Computer Science & Applied Mathematics, Weizmann Institute of Science, Rehovot, Israel.
2
Center of Advanced Technologies in Rehabilitation, Sheba Medical Center, Ramat Gan, Israel.
3
São Paulo State University (Unesp), Institute of Biosciences, Posture and Locomotion Studies Laboratory (LEPLO), Rio Claro, SP, Brazil.
Correspondence to: Paulo C. R. Santos
Department of Computer Science & Applied Mathematics, Weizmann Institute of Science, Rehovot, Israel
Weizmann Institute of Science - 234 Herzl St., PO Box 26, Rehovot, 7610001
email: paulocezarr@hotmail.com; paulo-cezar.rocha-dos-santos@weizmann.ac.il
https://doi.org/10.20338/bjmb.v16i5.353
ABBREVIATIONS
AD Alzheimer’s disease
PD Parkinson’s disease
CoM Center of mass
PUBLICATION DATA
Received 10 12 2022
Accepted 14 12 2022
Published 15 12 2022
ABSTRACT
Aging and age-associated neurological diseases, such as Alzheimer's disease (AD) and Parkinson's disease
(PD), may impair walking performance. Changes in walking performance are related to an increase in fall risk,
institutionalization, hospitalization, survival rate, and mortality. Due to the increase in the segment of the old
population and, consequently, in the number of individuals with age-related diseases, the amount of research
aiming at understanding the mechanisms underlying walking changes, examining tools to measure walking, and
developing interventions to improve walking performance in older individuals and in age-related diseases has
increased substantially. In this special issue, we target to compile information and strengthen the discussion about
whether and how aging and neurological diseases, specifically AD and PD, affect walking, and on potential
interventions to improve walking in these populations. A total of five studies compose this special issue, including
four original papers and one review.
KEYWORDS: Gait | Walking | Parkinson’s disease | Older people | Alzheimer’s disease
1. INTRODUCTION
Older population is growing drastically. World Health Organization projections
indicate that individuals aged over 65 years old will almost triple from 524 million in 2010 to
1.5 billion by 2050
1
. As the segment of the old population increases, incidences of age-
associated neurological diseases rise nearly parallel, being Alzheimer's disease (AD) and
Parkinson’s disease (PD) the most prevalent ones (4% and 1.1%, respectively)
2,3
. With the
increase in the number of older individuals and people with AD and PD, the consequent age-
, AD-, and PD-related declines in motor and cognitive functions are serious and growing
concerns for public health, and health and life sciences
1,4
.
As a consequence of those age-, AD- and PD-related declines in functions, the
capacity to maintain bipedal locomotion (i.e., ability to move from one place to another),
control postural stability, and adapt walking to different conditions (e.g., concomitant tasks,
or dealing with obstacles while perambulating) is affected in those populations. In this special
issue, we target to compile information and strengthen the discussion about whether and
how aging and AD, and PD affect walking (the most common way of human locomotion),
and potential interventions to improve walking in these populations. A total of five studies
compose this special issue, including four original papers and one review. The main findings
of these studies are briefly introduced in topics organized in ideas on how aging, AD, and
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PD affect locomotion, the role of walking task conditions (i.e., obstacle crossing and dual-
task), the mechanisms involved in gait stability and potentials interventions for walking for
older individuals and people with PD and AD.
2. AGING, AD, AND PD EFFECTS ON LOCOMOTION
Aging typically involves remarkable changes in walking, including spatial-temporal
(shorter and wider steps/strides, and slower walking speed) and neuromuscular control
(higher knee agonist-antagonist coactivation and lower synergistic ankle muscle coherence)
5–8
. Slowing speed is the most recognizable age-related change in walking (decreasing by
16% per decade from 60 years old). In AD and PD, those age-typical declines in walking
performance are even more evident (e.g., accentuated reductions in stride length and gait
speed, and increased gait variability in PD and AD compared to healthy older individuals)
9,10
. A decrease in walking performance overall, and walking speed in particular, is a hallmark
of health, as it predicts mobility independence, cognitive function, institutionalization,
hospitalization, survival rate, and mortality
11
. It is not a surprise that there is a substantial
growing of studies targeting understanding the underlying neural and associative
mechanisms of age-, AD- and PD-related decrease in walking performance, stability, and,
mainly, walking speed.
Regarding potential associative aspects related to poor walking performance,
Barbieri and colleagues
12
examined whether body composition of the lower limbs would be
associated with spatial-temporal walking parameters in people with PD. The rationale was
based on the idea that exacerbated sarcopenia (muscle loss) and osteopenia (bone mass
loss) in people with PD would somehow be linked to poorer walking performance. In fact,
the reduced lean and bone mass were related to slower gait speed in PD. This observation
points out that the potential cause of slow walking and stability may be multifactorial, but
certainly, the preservation of locomotion is related to the maintenance of body composition.
Another potential interpretation is that maintaining body composition would reflect
musculoskeletal plasticity, ensuring the neuromuscular control of walking and leading to
preserving walking speed and stability.
Following the hypothesis that aging would impair the capacity to modulate the
neuromuscular control to different walking speeds, Santos et al.
8
(intermuscular coherence)
tested the effects of aging and walking speed on intermuscular beta coherence. They
expected that age and walking speed would interact (e.g., older vs. younger individuals
would have lower coherence without modulating it with walking speed). Curiously, the
authors observed that aging but not walking speed affected intermuscular beta coherence
(also only between synergistic ankle but not thigh muscles). The authors also did not find
associations between speed-induced changes in spatial-temporal gait outcomes with
changes in beta coherence. Therefore, it is likely that other neuromuscular features (e.g.,
antagonistic coactivation
13
) instead of intermuscular beta coherence explain the age
differences in the neural control of walking speed.
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3. OBSTACLE AVOIDANCE AND DUAL-TASK WALKING CONDITION IN
AGING AND DISEASE
Due to the age-, PD- and AD-typical declines in cognitive functions, the capacity to
allocate cognitive resources to walk performing a concomitant secondary task (dual-task) is
affected
14–16
. This is supported by empirical data showing decreased walking performance
during dual-task walking
14–16
. Reasonably, the decline in either walking and/or cognitive task
may support the idea that cognitive function and walking are intrinsically linked
17,18
. Partially
supporting this idea, Costa et al.
19
compared longitudinally (32 months apart) the effect of
AD, mild cognitive impairment (MCI) on functional mobility (Timed Up and Go - TUG) isolated
and combined with a secondary test (dialing on the phone) with cognitively preserved
individuals. They found time-induced differences in time and cadence for both TUG
conditions and in the number of steps in dual-task TUG in AD vs. cognitively preserved, AD
vs. MCI, but not in MCI vs. AD. The results suggest that the progression of AD over time
affects, even more, the performance of walking, while in MCI, after three years, the
performance of mobility was virtually similar to the baseline. It partially reiterates the need to
maintain preserved cognition that certainly reflects “better” locomotion in older individuals.
Additionally, aging, AD, and PD affect the capacity to modulate walking to different
conditions of walking. A clear example is based on cumulative evidence showing that when
those populations need to negotiate with an obstacle, the risk of falls due to trips increases
substantially
20
. Trips during steps over obstacles are an eminent problem in healthy aging
and diseases since trips are one of the main reasons for falls
21
. The cause of the higher
number of trips in old age is still not fully elucidated, and studies are exploring potential
factors that increase the risk of trips and falls.
In this special issue, Becker and Rietdyk
22
quantified inadvertent trips and
differentiated factors present in those older individuals who tripped from those who did not.
They observed that 15 out of 41 older adults tripped while crossing obstacles at least once.
Those 15 individuals walked with slower walking speed, shorter stride length, higher
variability in the gait cycle time, indicated higher fatigue ratings, and took more medications
than those who did not have any trips. Therefore, walking performance during obstacle
avoidance can be a marker of the risk of falls. Even more, the presence of fatigue, as well
as the number of medications, may somehow be associated with trips and falls. Particularly
relevant, the present study supports the understanding of the circumstances related to trips
and the development of effective interventions to prevent trip-related falls in older individuals
22
. The authors also argued that whether the trip occurs with the leading or trailing limb may
be harder to control the center of mass (CoM) and restore stability during walking, which is
particularly challenging, as pointed out by van Leeuwen et al.
23
and discussed as follow.
4. MECHANISM TO CONTROL STABILITY DURING WALKING
Although trips and slips lead to a major number of falls in older individuals, the
occurrence of falls is somehow linked to the inability or difficulty to maintain (re)actively
dynamic stability. Walking stability requires a complex interaction of several mechanisms
23
that involves a net of functions affected by aging, and even more in AD and PD. Investigating
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those mechanisms, van Leeuwen et al.
23
proposed an overview of potential mechanisms of
gait stability control during unperturbed and perturbed walking. The focus of the review was
on detailing three mechanisms of walking stability: (1) foot stability, (2) stance leg control,
and (3) angular momentum changes. Briefly discussing each mechanism, firstly, to stabilize
walking in the mediolateral direction, the foot placement should be lateral to the extrapolated
CoM position, while for anteroposterior, the foot placement seems to be dependent on the
anteroposterior pelvis velocity with mediolateral pelvis position and velocity. Secondly, by
ankle movements (inversion/eversion and plantar/dorsiflexion), stance leg control can
modulate the center of pressure shift in both mediolateral and anteroposterior directions.
Thirdly, the angular momentum can be used to stabilize walking to a certain extent,
suggesting a relatively minor role in controlling the CoM.
In aging and age-related diseases, errors in foot placement, changes in pelvis
velocity and movement, limited active control of ankle movements, or even the typical
changes in steps metrics (width, length) may reflect in the reduced stabilization of walking.
For instance, by increasing step width, typically observed in older and PD individuals, the
strength of the coupling of the mediolateral CoM state and foot placement may decrease
24
.
Additionally, as also mentioned by van Leeuwen et al.
23
, sensing and actuation of those
mechanisms are strictly relevant to actively controlling stability during gait. As both sensing
and actuation are diminished in aging and diseases, these factors combined may partially
explain the reduced control of gait stability in those populations. Thus, understanding how
walking is stabilized, combined with the information of the studies composing this special
issue, can support optimizing training targeting aging and age-related disease populations.
5. POTENTIAL INTERVENTIONS AND FUTURE DIRECTION
One of the main clinical relevance of understanding the mechanisms and factors
linked with whether and how age- and age-related diseases affect walking is centered on
developing or optimizing intervention strategies (e.g., prevention and rehabilitation). Not
differently, papers composing this special issue suggested
12,22
, or even directly indicated
23
,
training strategies for general or specific aspects related to improving walking. Barbieri and
colleagues
12
suggested that exercise programs focusing on maintaining body composition
(especially with a mechanical load) would reflect in the maintenance of walking speed and
stability. Becker and Rietdyk
22
also briefly mentioned, because of the link between fatigue
increasing the risk of trips, the relevance of intervention programs in improving endurance
capacity. Those suggestions confirm the cumulative and systematic evidence on exercise
effectiveness on walking ability, improving performance, and reducing falls in older and PD
individuals
25,26
. Specifically considering intervention focusing on the mechanisms of gait
stability, van Leeuwen et al.
23
discussed detailed strategies to improve foot placement and
stance leg control. The authors suggested that mechanically perturbed gait stability,
specifically perturbed or augmented use of stabilizing mechanisms, may be potential training
approaches for improving gait stability.
Even when not directly suggested, we still can use the information from the studies
published in the special issue to raise potential strategies of intervention in old and AD
populations based on the studies of Santos et al.
8
and Costa et al.
19
Considering that aging
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seems to affect the strength of synaptic inputs (inferred by intermuscular beta-coherence) to
ankle, but not thigh, muscles during walking
8
, intervention mainly focusing on the ankle
muscle seems to be more relevant for older individuals. Indeed, improving ankle functions
may be relevant, considering that this can also be beneficial for foot placement (a
mechanism of gait stability
23
) and because of the typical distal-to-proximal redistribution of
joint work during walking in older adults
27
. Also, since exercise-induced neuroplasticity is
associated with improvements in motor function
28
, enhancing physical activity level may
reflect in the strength of synaptic inputs optimizing the motor control, reducing the negative
effects on intermuscular beta coherence. Exercise as an intervention is also important to
reduce the progression of the disease and improve cognitive-motor function in AD
29
. Thus,
extending for discussing around the results of Costa and colleagues
19
, we can interpret that
exercise would avoid or minimize the interference of the cognitive decline of AD, reflecting
in lesser decline in mobility (alone or in dual-task conditions).
In light of all findings, this special issue proposes an overlook on whether and how
aging, AD, and PD affect gait, targeting to contribute to strengthening the discussion on the
age-, PD- and AD-related factors and mechanisms that can interfere with walking, and on
potential intervention strategies that can improve walking in those populations.
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Citation: Santos PCR, Orcioli-Silva D (2022). Editorial: Effects of aging on locomotor patterns. Brazilian Journal of
Motor Behavior, 16(5):319-325.
Editor-in-chief: Dr Fabio Augusto Barbieri - São Paulo State University (UNESP), Bauru, SP, Brazil. !
Associate editors: Dr José Angelo Barela - São Paulo State University (UNESP), Rio Claro, SP, Brazil; Dr Natalia
Madalena Rinaldi - Federal University of Espírito Santo (UFES), Vitória, ES, Brazil; Dr Renato de Moraes – University
of São Paulo (USP), Ribeirão Preto, SP, Brazil.
Guest editors: Dr Paulo Cezar Rocha dos Santos - Weizmann Institute of Science, Rehovot, Israel; Dr Diego Orcioli
Silva - São Paulo State University (UNESP), Rio Claro, SP, Brazil.
Copyright:© 2022 Van Leeuwen, Bruijn and van Dieën and BJMB. This is an open-access article distributed under the
terms of the Creative Commons Attribution-Non Commercial-No Derivatives 4.0 International License which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-
profit sectors.
Competing interests: The authors have declared that no competing interests exist.
DOI:!https://doi.org/10.20338/bjmb.v16i5.353
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