Neuromuscular Gait Research, Disability and Age

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BioMechanics July 2005 www.biomech.com

Engineering efficiency: Geriatric gait research goes tech

By: A. McGibbon, PhD

Mobility impairments have a profound effect on health-related quality

of life. Limitations in function, primarily caused by impairments of

organ and body systems, often lead to disability,1,2 broadly defined

as the inability to maintain one's vocational and avocational life

roles.3 The relationship between lower extremity musculoskeletal

impairments (e.g., muscle weakness, limited range of motion, or pain)

and functional limitations (e.g., the inability to climb stairs, or

walk more than a short distance) often manifests as an abnormal

locomotor pattern. A logical conclusion is that changes in locomotion

are driven by neuromuscular adaptations, which alter how the body

moves to reduce the effects of impairments on physical function.

Unfortunately, the benefits of these adaptations can be offset by

increased risk of secondary pathology or instability leading to

falls. As shown in Figure 1, adaptations may take the form of

compensations in response to impairments, existing to replace lost or

diminished function of surrounding structures, such as hip muscles

acting to compensate for diminished function of ankle muscles. Or

they may themselves present as impairments, such as reduced ankle

power output due to reduced ankle muscle strength. While the effects

of adaptations and compensations can often be observed in measured

locomotor patterns, the underlying neuromuscular mechanisms that

arise from musculoskeletal pathology are neither well documented nor

well understood.

Modern motion tracking systems and recent advances in

neuromusculoskeletal modeling offer a promising avenue for better

understanding the underlying mechanisms that cause functional

limitations and lead to disability. A review of some of the research

studies that have laid the foundation for better understanding gait

dysfunction in older adults may enhance discussion of some of the

emerging areas of biomechanical research that hold promise for

rehabilitation of older adults with gait dysfunction.

Effects of age on gait

Several age-related conditions are known to contribute to diminished

gait function: reduced muscle strength4,5 and an associated decline

in torque- and power-generating capacity;6-8 subtle deterioration of

sensory systems, including the peripheral (vestibular) and central

(cerebellar) postural control systems;9,10 diminished cardiovascular

and respiratory function;11 and psychological factors such as

depression and fear of falling.12,13 Observable characteristics, such

as decreased walking speed, widened base of support, and shortened

stride length,12-15 are due in part to a combination of the above and

other factors associated with aging. Recent studies suggest that

biomechanical analyses of gait, using kinematic and kinetic analysis

techniques (primarily of angular rotations, moments, and powers), can

illuminate the mechanistic behaviors responsible for these changes in

gait with aging16-21 and disability.21-27

Studies of age-related changes in gait report reductions in ankle

plantar-flexion and plantar-flexor moment and power,16-19,21 reduced

knee flexion and knee-extensor moment and power,16,19 reduced hip

extension,18,20,28 increased hip-extensor or -flexor moment and

power,17-19,21 and altered trunk-pelvis coordination25 in healthy

elders compared to young adults. Studies examining the biomechanics

of gait in disabled populations (such as subjects with knee

arthritis) show many of the same characteristics as those documented

in healthy aging populations, with some potentially important

differences, however, one being a dramatic increase in hip-flexor

power absorption.21,23,26 A recent review article21 discusses some of

the above studies in more detail, providing several plausible

mechanistic explanations for neuromuscular adaptations in the gait of

persons 65 and older.

These patients demonstrate, among other differences, a significantly

lower plantar-flexor power " burst " in the terminal stance phase of

gait when compared to young adults. Winter et al16 interpreted the

ankle plantar-flexor power burst as a " pistoning effect, " providing a

mechanism to assist in forward progression of the whole body and

stabilization of the upper body. The same group also reported an

increase in knee power absorption in late stance for elderly walkers,

suggesting that the knee acted to prevent power from transferring

proximally. Others have suggested that ankle power contributes not

only to forward progression of the body, but also to advancement of

the leg into swing phase.20,29,30 Rapid ankle torque generating

capacity decreases with age, thereby representing a potential

impairment that limits gait function in elders.7 Dynamic simulations

recently reported by Neptune et al30 suggest that impaired plantar-

flexor function may affect trunk stabilization in early stance phase

of gait, and trunk progression and swing initiation in late stance

phase. It follows that impaired ankle plantar-flexor function would

require a compensatory response from other muscles to stabilize the

trunk and assist with forward progression of the trunk and swing leg.

Identifying the underlying mechanism(s) leading to reduced vigor of

gait (measured primarily as gait speed) with age has been a focus of

several studies. Judge et al29 reported that the difference in ankle

power between young and elderly persons could explain stride length

differences, but that elderly individuals generate more hip flexor

power for their walking speed than do healthy young adults. This

suggests that diminished ankle plantar-flexor function potentially

limits gait speed, requiring hip flexor concentric action to

compensate by pulling the leg forward to assist with swing

initiation. In contrast to Judge's29 study, Kerrigan et al18 found

that hip power was not increased while ankle plantar-flexor power was

with faster walking speed in elderly persons compared to young

adults. Older subjects also significantly increased their hip

extensor moment in early stance phase when walking at their maximal

pace. In addition, reduced maximal hip extension for these subjects

was reported, which Kerrigan et al18 attributed to hip flexion

contracture.

While Judge's study suggested that diminished ankle plantar-flexor

function is the primary age-related impairment affecting gait,

Kerrigan's study suggested that hip flexor contracture is the primary

age-related impairment affecting gait; both impairments affect step

length and gait speed, but clearly by different mechanisms. While the

results of these two studies present fairly divergent theories of

diminished gait function in older people, it is perhaps important

that this is so, suggesting that different impairments may have

similar effects on gross gait function (reduced speed and step

length) though they emanate from very different neuromuscular

adaptations.

DeVita and Hortobagyi19 explored age-related neuromuscular

adaptations in gait by comparing joint kinematics and kinetics of

healthy young adults and elderly individuals, where both groups had

equal self-selected gait speed. Geriatric subjects demonstrated

greater hip extensor moment and power and reduced hip flexor moment,

knee extensor moment and power, and ankle plantar-flexor moment and

power compared to young subjects. Importantly, however, the support

moment (sum of ankle, knee, and hip moments16) was equal for the two

groups, suggesting a redistribution of muscle moment and power that

occurs with aging. A shift in the locus of neuromuscular function

with aging supports the notion that hip musculature adapts to

compensate for decreased function of distal joint muscles by

increasing efforts to control and stabilize the trunk. That

differences existed in ankle plantar-flexor power between elderly and

young groups walking at the same speed contradicts the findings of

Judge et al29 but indirectly supports the findings of Kerrigan et

al.18 Conversely, DeVita and Hortobagyi's study did not show a

decrease in hip range of motion, which contradicts the hip flexor

contracture theory suggested by Kerrigan.

As suggested earlier, the differences between the above studies

exploring the age-related decline in gait function may be more

important than their similarities. In other words, these differences

might be explained by different combinations of impairments possessed

by the elderly groups studied, and as such, need to be quantified in

relation to the observed neuromuscular adaptations.

Effects of disability on gait

While providing a wealth of information on the possible mechanisms of

neuromuscular adaptation in the elderly, the above studies included

only elders considered healthy (at least by subject self-report and

sometimes medical screening), and thus it is highly probable that

undocumented impairments explain, at least in part, some of the

discrepancies among studies. Unfortunately, far fewer studies have

examined the biomechanical characteristics of gait in a sample of

elders with known impairments.

McGibbon et al24 examined the effects of pathology (classified as

musculoskeletal, nonmusculoskeletal, and nonspecific) and strength

(classified as weak, moderate, and strong), on joint motor function

in gait for a sample of 75 functionally limited elderly women. Weaker

subjects expended less mechanical energy at the ankle and knee

regardless of pathology. Weaker subjects with musculoskeletal

pathology expended more mechanical energy at the hip and low back

than did stronger subjects with musculoskeletal pathology. Excessive

hip flexor21,23,26 and low back extensor,23 power absorption, or

eccentric work during gait appears to be prevalent in geriatric

patients with lower extremity impairments, but not in healthy

elders.17-19,11 McGibbon et al23 showed that low back and (when

controlling for gait speed) hip energy expenditures were greater for

elderly subjects with lower extremity impairments (due to a variety

of pathologies) compared to healthy age-matched subjects.

As a follow-up to this study, McGibbon and Krebs26 applied the same

analysis as in prior reports23,24 to a more homogenous sample of

elderly individuals having unilateral knee osteoarthritis. The OA

patients had significantly increased eccentric hip flexor work, and

also significantly reduced concentric ankle work in late stance phase

and knee work in mid- to late stance phase, compared to age-matched

healthy elders. The increase in hip eccentric power is interesting in

light of Kerrigan's study18 implicating hip flexion contracture as a

limiting impairment with aging. It is plausible that the OA patients

could take advantage of tight hip flexors, relying on quadriceps

stretch reflex, or passive elastic properties, to help advance the

leg into swing phase or assist in the propulsion of the upper body,

as illustrated in Figure 2.

In a recent study McGibbon and Krebs21,31 sought to identify the

biomechanical variables indicative of lower extremity dysfunction

that are distinct from age-related gait adaptations, and the

interrelationships among these variables, to better understand the

underlying mechanisms of neuromuscular adaptations in gait. Ankle,

knee, and hip peak angles, moments, and powers in the sagittal plane

were acquired during gait at self-selected speed in 120 subjects

(healthy young, healthy elders, and elders with lower extremity

musculoskeletal pathology).

Discriminate analysis was used to identify the key biomechanical

variables discriminating by age (young or old and healthy) and by

health status (healthy or disabled and old). Healthy older subjects

were discriminated (sensitivity/specificity = 76%/82%) from young

subjects via decreased late-stance ankle plantar-flexion angle, and

increased late-stance knee power absorption and early-stance hip

extensor power generation. Disabled elderly subjects were

discriminated (74%/73%) from healthy ones via decreased late-stance

ankle plantar-flexor moment and power generation, increased early-

stance ankle dorsiflexor moment and late-stance hip flexor moment and

power absorption.

Most importantly, the relationships among these variables showed a

high degree of coupling for the disabled elderly subjects compared to

the young and elderly healthy subjects (Figure 3), suggesting a

reduced ability for elders with lower extremity impairments to alter

motor strategies. The data suggest that older patients with lower

extremity dysfunction rely excessively on hip flexor passive action,

probably to provide propulsion in late stance, and ankle dorsiflexors

of the contralateral limb to provide leg and trunk stability. The

passive hip flexor theory, however, is weakened somewhat since hip

flexion range was not a significant variable in the model, indicating

that hip flexion contractures were not significant in the disabled

geriatric patients. More detailed studies of these compensatory

mechanisms are required.

The studies above suggest that it is possible to quantify

neuromuscular adaptations in the elderly. But these studies also

suggest that underlying impairments responsible for the adaptive-or

maladaptive-compensations are critically important to consider when

assessing neuromuscular function in these patients. The fact that

this has not been done is the most likely explanation for why we

still know so little about gait dysfunction in older patients. To

date, there are no comprehensive studies that document neuromuscular

function in a large sample of elderly subjects with a wide range of

documented impairments. The ability to predict neuromuscular

adaptations from existing impairments would greatly enhance the

development of physical therapy interventions to aid the disabled.

Neuromusculoskeletal modeling

The majority of studies aimed at better understanding the

neuromuscular basis of gait dysfunction in elderly patients have

relied upon standard and easily implemented biomechanical analysis of

the joints: moments, powers, and energies, all based on inverse

dynamics. All the papers discussed above have relied on these

analysis techniques. There are limitations to these approaches,

however.

First, inverse dynamics can inform us only about the " net " effect of

muscle interactions, providing no information about the role of

individual uniarticular and biarticular muscles. Second, we are

unable to determine how individual muscles (or even net joint

moments) influence the kinematics of body segments not directly

connected to the joint being studied. And third, we cannot make

conclusions about alternate control strategies that might improve

function. These points are especially important in terms of

rehabilitation engineering of motor dysfunction. It has become

increasingly clear that more sophisticated biomechanical techniques

are needed to overcome these limitations. Fortunately, these

techniques already exist, though they have yet to be applied to

disabled elders.

The techniques referred to above fall into a class of biomechanics

known as forward dynamic analysis, or dynamic simulations. They

differ from inverse dynamic analysis in the sense that the inverse

approach seeks to determine the joint moments and forces that explain

the motions observed, while the forward approach seeks to determine

the motions that occur given the forces and moments at the joints.

Taken one step further, we can also use muscle models to distribute

the net joint force and moments into individual muscle and joint

contact forces (using an inverse approach), or we can specify muscle

excitations and compute the body segment motions that result (using a

forward approach). This latter approach is generally called

neuromusculoskeletal modeling. A detailed description of this

approach can be found in several recent publications.32-35

Forward dynamic simulations and neuromusculoskeletal models have been

used primarily in healthy normal populations to better understand

muscle function and coordination,36-39 but several recent studies

have demonstrated their usefulness in predicting surgical outcomes

for children with stiff knee gait associated with cerebral palsy.40-

42 Once a muscle model and simulation are built for a specific

patient, alterations can be made to the model (such as changing the

muscle's insertion with a tendon transfer) and the effect of these

alterations on gait can be simulated. One area of clinical interest

may be for treatment of hip flexor contracture in older adults. As

suggested by our prior studies, eccentric hip flexor work is much

greater for elders with general lower extremity impairments. Are

patients taking advantage of tight hip flexors as a passive mechanism

to aid in stance limb advance in swing phase? If so, does this result

in increased hip loads? How should this compensatory strategy be

modified (assuming it should be!)? Soon simulations may be able to

answer these questions for individual patients.

Engineering to move forward

While these modeling and simulation techniques are not free of

problematic issues (see Hatze43,44 for a discussion of these issues),

they hold promise for rehabilitation engineering of gait disorder in

older adults, as recently demonstrated in a simulation for better

understanding muscle control in slow gait.45 In my opinion, when we

better understand the relationships among impairments and the

underlying neuromuscular adaptations, then subject-specific

neuromusculoskeletal models may be the best hope for deciding how to

modify impairments, simulate the outcomes of these modifications on

gait, and better prescribe treatment options for alleviating the

functional limitations that lead to disability in a growing elderly

population.

A. McGibbon, PhD, is a professor kinesiology and the research

chair in rehabilitation biomechanics at the Institute of Biomedical

Engineering at the University of New Brunswick in Fredericton, NB.

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