University of Groningen Effects of lower extremity power training on gait biomechanics in old adults Beijersbergen, Chantal

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Effects of lower extremity power training on gait biomechanics in old adults Beijersbergen, Chantal

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Chantal M.I. Beijersbergen

Urs Granacher

Anthony A. Vandervoort

Paul DeVita

Tibor Hortobágyi

Ageing Research Reviews 2013 March;12(2) 618-627

Chapter 2

The biomechanical mechanism of

how strength and power training

improves walking speed in old

adults remains unknown

Chantal Beijersbergen

Urs Granacher

Anthony Vandervoort

Paul DeVita

Tibor Hortobágyi

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Abstract

Maintaining and increasing walking speed in old age is clinically important because this activity of daily living predicts functional and clinical state. We reviewed evidence for the biomechanical mechanisms of how strength and power training increase gait speed in old adults. A systematic search yielded only four studies that reported changes in selected gait biomechanical variables after an intervention. A secondary 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 R2_{= 0.16 between the 19% and 9% gains in plantarflexion strength and}

gait speed in 240 old volunteers age 75. In 8 studies, there was zero association between the 35% and 13% gains in leg mechanical power and gait speed in 150 old adults age 73. To increase the efficacy of intervention studies designed to improve 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.

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2.1. INTRODUCTION

Aging, whether along healthy or non-healthy paths, modifies human gait. While aging after age 50 modifies many gait characteristics, shorter steps and slower walking speed may be the most functionally meaningful. The magnitude of the reductions in step length and walking speed are associated with the magnitude of any decline in health while aging. Consequently, self-selected habitual gait speed measured on a level surface is a marker and predictor of many clinical conditions, including daily function, late-life mobility, independence, falls, fear of falls, fractures, mental health, cognitive function, adverse clinical events, hospitalization, institutionalization, and survival [1–11]. Gait speed in old adults, i.e., age over 70, that is similar to young adults’ speed signifies multi-systemic wellbeing and slowed gait suggests clinical or sub-clinical impairments [12].

Usual gait speed decreases up to 16% per decade starting already at age 60 [1,12–15]. Many old adults’ usual gait speed decreases to the functionally inadequate levels of 0.8 m/s and even slower [1], signifying mobility disability. The slowing of gait perpetuates physical inactivity because the time needed to cross the street or reach a destination becomes too long and old adults lose motivation to ambulate [16]. Step length shortens and gait speed slows due to sarcopenia, dynapenia, reduced joint range of motion, weakness, fatigue, and lower dynamic stability [12,17–19]. Additional reasons for short step length and reduced gait speed are the desire to walk with a greater sense of stability and the strategy to avoid high forces causing joint pain [1]. Maintaining usual gait speed in old age is of major clinical and functional significance as it is clear that old individuals with faster usual and maximal gait speeds have greater longevity [1,8,20]. Further, although as yet not directly proven, these crosssectional studies support the attractive hypothesis that increasing step length and gait speed may even increase longevity.

Unsurprisingly there is a massive ongoing preventative effort to improve old adults’ abilities to successfully perform activities of daily living (ADLs) (e.g., [21]). Within this effort a clear target is to slow the rate of gait speed loss in healthy old adults and to restore gait speed in those patients who suffer from mobility disability and such other clinical conditions as cancer, neuropathy, and osteoarthritis. Numerous interventions, applying resistance, power, balance, and specific locomotor training have demonstrated remarkable increases in maximal voluntary muscle strength and power up to 85% and as much as 53% in gait speed [4,22]. The common element of the intervention studies that provides the pretext for this review is a complete absence of addressing the mechanisms of how interventions increase gait speed in old adults. Although clinicians routinely prescribe interventions for old adults [21], we do not know how, if at all, does the intervention-improved physical capacity become incorporated into the movements of ADLs and in case of gait, produces longer steps and faster walking. Although a handful of studies did examine how specific interventions affect selected biomechanical variables in relation to gait speed, no studies to date have reported the association between

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improvements in maximal voluntary strength and power and the improvements in lower extremity joint kinetics and energetics, identifying the mechanisms behind intervention-induced improvements in gait speed. The aim of the present review was to draw attention to a critical gap in our understanding as to how interventions improve mobility functions in old adults in general and, in particular, how strength and power training improve gait speed in old adults. We addressed the question, ‘What is the biomechanical mechanism of interventions increasing gait speed in old adults?’ First we review the age-related reorganization of mechanical output at the hip, knee, and ankle joints during gait and link these torques to the maximal torque available in the lower extremity joints. Finally, we review the effects of strength interventions on gait biomechanics, summarize the potential mechanisms, and make recommendations for future research.

2.2. AGE-RELATED MECHANICAL PLASTICITY OF GAIT: A DISTAL-TO-PROXIMAL SHIFT IN MUSCLE FUNCITON

2.2.1. Walking kinematics

Healthy aging after age 50 produces profound modifications in gait. Step length, step rate and their product, walking velocity, are fundamental sagittal plane biomechanical descriptors of walking. Self-selected walking velocity is lower in old (~1.15 m/s) compared with young (~1.32 m/s) adults [15,23–27]. This decline in walking velocity is associated with reduced step length [24–26,28–31] and increased step rate or cadence [23]. The increase in cadence however is not sufficient to offset the decrease in step length, thereby reducing velocity. Furthermore and as a consequence of reduced step length, double support time increases with concomitant reductions in single support and swing times [32,33]. It is thought that these latter adaptations increase dynamic stability in the elderly [33]. Whereas more recent studies suggest that another strategy to improve stability with aging is a wider support base or step width [34]. Overall, it is well documented that basic gait kinematics, including walking velocity and its related factors, are changing with age.

Locomotion biomechanics have been compared between young and old adults while walking at both identical and different, self-selected walking velocities. Both comparisons are important and identify different aspects about locomotion biomechanics in old adults. Self-selected velocities are more ecologically sound and identify behaviorally meaningful age-related differences in gait. The slower walking speed typically selected by old adults manifests itself in lower joint torques and powers and these directly produce shorter steps and lower velocity [33]. Due to the shorter steps, old adults also produce less work per step [31]. Matched velocity comparisons on the other hand have value because these show neuromuscular adaptations strictly due to aging physiology without the confounding effects of age and velocity. We note that while horizontal velocities are often monitored or controlled in these studies, vertical kinematics are typically completely unmonitored and unconstrained (but see

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[35]). Differences in vertical displacement profiles between young and old, for example, would be a direct outcome of differences in muscle work and would be associated with different metabolic and mechanical costs of walking. While the observed age-related gait differences such as the increased metabolic cost of walking in old adults may be related to altered neural activation during gait [36,37], it is possible that such differences are also due to vertical kinematics [22,34].

2.2.2. Effects of age on hip joint function during gait

Comparisons made at both identical and different velocities have shown significant changes with age in joint kinematics and kinetics at the hip, knee and ankle joints. Old compared with young adults show greater range of motion at the hip throughout each gait cycle [33,38,39]. Along with greater hip range of motion, old adults walk with larger internal hip extensor torque and positive power in early stance phase and more internal hip flexor torque and positive power during late stance compared with young adults [33]. The duration of the hip extensor torque and power generation was also longer in old compared to young adults, producing larger total angular impulse and work at the hip [33]. Overall, old adults increase hip range of motion, torque, power and work during walking compared to young adults when gait velocity is matched. In fact, it appears that a wider step width (i.e., more dynamic stability) is associated with increased hip muscle activity without concurrent changes in the activation of ankle evertors and invertors [40]. Further, increased hip joint function with age was also important for increasing walking velocity. Old adults increased their walking velocity from comfortable to fast pace by increasing the internal hip extensor torque and positive power in early stance or their hip flexion torque and positive power in late stance [23,24,41].

2.2.3. 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 compared with young adults [33]. Reduced flexion in early stance was the primary kinematic adaptation producing the more erect walking pattern with a lower knee extensor torque seen in old adults. Adaptations in knee torque as a consequence of age are inconsistent: knee extensor angular impulse during early stance, representing knee extensor torque, was lower in one [33] but similar in another study [26]. In fact, when normalized to mass and height, old adults walked with greater knee extensor torque and concomitant negative work and negative peak powers during loading response [42]. 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 positive and negative work, and therefore less power output at the knee in one case [33], whereas others reported greater power output for old compared with young adults [26,38,42]. Additional studies are needed to

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resolve these clinically critical inconsistencies in knee function during gait. 2.2.4. Effects of age on ankle joint function during gait

In contrast to the findings on knee biomechanics, mechanical changes at the ankle joint during walking and due to age are highly consistent within the literature [43]. Old vs. young adults maintain their position of the foot closer to the anatomical position during stance phase and they show less range of motion in the gait cycle [33]. Many studies reported old adults to walk with a reduced plantarflexion peak position just before push-off [24,33,38,39,42] and also with a reduced plantarflexion torque during late stance [33] compared with young. Furthermore, it is clearly reported that healthy old adults have reduced ankle plantarflexor power output during push-off compared with their younger counterparts when gait speeds are matched [33,38,42]. Ankle power generation during push-off plays an important role in forward progression of the body, and consequently the reduction in stride length and increased double leg support that occur with increasing age can be at least partially attributed to the reduction in power production of the calf muscles.

Overall old adults use lower plantarflexor torque and generate less positive ankle power during push-off and there is a concurrent increase in peak hip extension power during early stance and peak hip flexor power generation during late stance. Fig. 2.1 shows this “redistribution of joint powers” and the overall distal to proximal shift in muscle function, a phenomenon coined as the age-related mechanical plasticity of human gait [33]. Numerically, there was an 19% reduction in mass-normalized ankle power and 38% increase in hip power as healthy volunteers walked at a range of speeds between 1.0 and 1.5 m/s in 8 studies [23,24,26,36,38,39,42,44] (Table A.1 in Appendix A).

In summary, these data illustrate that there are multi-focal age-related adaptations in gait kinematics and kinetics. Next we review the evidence for strength interventions causing adaptations in gait biomechanics and increases in old adults’ gait speed.

Figure 2.1. Mechanical plasticity of old adults’

gait. Body mass normalized hip, knee, 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 adults. Joint powers were recorded under 6 walking conditions ranging in walking speed between 1.0 and 1.5 m/s in 7 studies. * P = 0.050 at hip and P = 0.022 at ankle between young and old adults. Hip Young Old 5.0 4.0 3.0 2.0 1.0 0.0 Joint po w er , W/kg Knee Ankle * *

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2.3. SCANT BIOMECHANICAL EVIDENCE FOR HOW STRENGTH INTERVENTIONS INCREASE GAIT SPEED

Based on 55 studies, a previous review analyzed the effects of exercise interventions on locomotor function in old adults [22]. The nature of interventions varied widely and included strength, power, balance, flexibility, aerobic, and mobility exercise protocols or combinations thereof. Most studies used selfselected gait velocity as a primary outcome to quantify the effects of an intervention along with performance-oriented tests such as fast walking velocity, stair climbing velocity, 6-min walk distance, and up-and-go test time. As expected, self-selected velocity increased 14% and the time to perform the walking tests decreased 12%, suggesting that old adults adapt and benefit from exercise therapy through improvements in spatio-temporal gait characteristics [22]. However, the review also highlighted the remarkable omission in the literature as to how little we know about the biomechanical mediators of increased walking velocity associated with exercise interventions, a mechanism that remains unknown today.

2.3.1. Search toward effects of specific strength and power training on gait characteristics

To address the issue of biomechanical mediators and extend the previous review [22], we conducted a systematic literature search up to November 2012 using the following terms in the MEDLINE and COCHRANE search: (“aged [MeSH]”) AND (“gait [MeSH]” OR “locomotion [MeSH]” OR “walking [MeSH]” OR “ambulation [Text Word]”) AND (“exercise [MeSH]” OR “resistance training [MeSH]” OR “power training [Text Word]”) AND “biomechanics [MeSH]” OR “kinetics [MeSH]” OR “power [Text Word]” OR “joint [Text Word]”. The search was limited to English language and age ≥ 65. Duplicates appearing in both searches were removed. Fig. 2.2 summarizes the searches.

2.3.2. Selection criteria

Studies were included in the review if: (a) study participants were aged ≥ 65 years; (b) performed strength or power intervention (except otherwise stated due to a limited number of studies available), and (c) if a study incorporated at least one gait biomechanical outcome measure. Studies were excluded if: (a) participants had a history of neurological disease, (b) participants were amputees or used prosthesis; or (c) they were not written in English. Based on these criteria, we analyzed the abstracts of any potentially relevant papers and performed accordingly content analysis of the full paper. 2.3.3. Quality assessment

Two reviewers assessed the methodological quality of the included studies using the Physiotherapy Evidence Database (PEDro) scale. The PEDro scale rates randomized controlled trials from 0 to 10 with a score above 6 representing high quality [45].

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2.4 RESULTS

The flow chart in Fig. 2.2 summarizes the systematic review. The search identified 724 studies (MEDLINE n = 669; COCHRANE n = 55). After the elimination of 30 duplicates and 675 studies based on title or abstract, additional 15 studies were eliminated based on eligibility criteria. In the end, four studies met the inclusion criteria and were retained for analysis.

2.4.1. Quality assessment

The mean quality score for the 4 included studies was 5.5 ± 2.4 (range, 2–7). We included a single arm study without a control group, scoring only 2. The other three studies had a PEDro score between 6 and 7, suggestive of high quality [35,46,47]. 2.4.2. Evaluation of the four intervention studies identified by the systematic search

Hartmann et al. examined the effects of a 12-week strength training program with and without foot gymnastics on muscle strength and gait kinematics measured with a trunk accelerometer in healthy old adults age 76 [46]. Knee and ankle strength increased 14–46% (P < 0.05) and gait parameters improved 1–11%, with gait speed and step length improving similarly 6.6% and 5.0% in the two groups (P < 0.05). The training program supplemented with foot gymnastics increased ankle range of motion to 11.9° from 11.1° (P = 0.036). The authors did not compute or report the association between changes in strength and gait kinematics.

Persch et al. observed that 12 weeks of strength training improved maximal isometric strength of the hip, knee, and ankle muscles 60% and also increased step length (0.14 m), gait speed (0.13 m/s), and cadence (11 steps/min) (all P < 0.05) in healthy adults age 61 [35]. After strength training, subjects struck the ground with 3.7°, 2.6°, and 1.1° more peak hip, knee, and ankle flexion and walked with 5.6°, 0.8°, and 4.0° more hip, knee, and ankle range of motion in the stance phase (all P < 0.05). Despite the larger flexion in the lower extremity joints, somewhat paradoxically, the vertical displacement of the center of mass decreased 8 mm (P < 0.01), suggesting a less dynamic albeit faster gait. Changes in plantarflexor strength were associated with changes in cadence R2_{= 0.30 (P < 0.05) but not with changes in gait speed. Changes}

in knee extensor strength correlated with changes in stride length R2_{= 0.44 (P < 0.05)}

and changes in hip flexor strength correlated with changes in stride length R2_{= 0.17 (P}

< 0.05). Thus, improved knee extensor function through training plays a relatively more important role in improving gait speed than changes in ankle and hip flexor function.

McGibbon et al. compared the effects of 6 weeks of strength or functional training in small samples of old adults age 75, with at least one lower extremity impairment [47]. Functional training improved leg strength (26%) significantly more than strength training (16%). Functional training improved gait velocity significantly (P = 0.001) more (0.178 m/s increase) than strength training (0.055 m/s increase).

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Ankle kinetics during gait improved 56% in the functional training group and 9% in the strength-training group (difference P = 0.024) as measured by ankle plantarflexor mechanical energy expenditure but only the functional group improved knee kinetics 108% compared with 27% decrease in the strength-training group (difference P = 0.038). Hip extensor mechanical energy expenditure decreased 10% after functional but increased 97% after strength training (difference P = 0.053). Although improvements in gait were similar in the two groups, the authors concluded that improved coordination of muscle power mediated the improved mobility in the functional group. The authors did not compute or report the association between changes in strength and gait kinematics and kinetics.

Cao et al. showed that a 12-week-long intervention consisting of aerobic, balance, strength, coordination, and walking exercises did not improve step length and

MEDLINE Library

Limits; English-language articles only (n=669)

COCHRANE Library

Limits; English-language articles only (n= 55)

Duplicate articles excluded (n=30) Articles screened based on title

and abstract (n=694)

Articles included for full text analysis (n=19) Included articles (n=4) Articles excluded (n=675); - Non-exersise study (n=604) - Neurological Disease (n=27) - Osteoarthritis (n=13) - Amputee or prosthetic (n=11) - Diabetic (n=2) - Age <65 years (n=4) - Other (n=14) Articles excluded (n=15);

- Lack on biomechanics report (n=14) - One-day exercise program (n=1)

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gait velocity. However, old adults’ gait became more dynamic as they walked with more hip flexion at heel-contact and toe-off in the stance and through the swing phase [48]. Further, there was more knee flexion at heel-contact and during swing-phase and more ankle plantarflexion at toe-off. The dynamic range of motion at the ankle increased 3.7º (P < 0.05). Even though the authors used the 30-s chair stand test to indirectly measure leg strength, they attributed the changes in gait kinematics to improvements in ankle strength. The authors did not compute or report the association between changes in strength and gait kinematics.

2.4.3. Association between improvements in gait speed and muscle strength and power

Based on an extensive search and analysis of the literature, we found limited biomechanical evidence to explain how interventions in general and strength and power training in particular improve walking speed in old adults. Current evidence is insufficient and inconsistent to explain how and if at all newly acquired strength and power become incorporated in the locomotor muscles that drive the limbs during gait. In lieu of kinematic and kinetic gait data, we argue that the next best available evidence to determine if improved muscle strength is a moderator of increase in gait speed is to quantify the association between improvements in gait speed and gains in muscle strength and power.

We were able identify 4 studies that reported such correlations. Judge et al. reported R2_{= 0.31 (P > 0.05) association between leg strength and gait speed in 31}

community-dwelling adults age 82 before a strength training intervention and stated that this association did not change after the intervention, suggesting no independent role for muscle strength in improving gait speed [49]. Persch et al. observed an association of R2

= 0.44 (P = 0.001) and R2_{= 0.17 (P = 0.049) between changes in knee extensor and}

hip flexor strength, respectively, and stride length (thus indirectly with gait speed) in 14 old adults age 61 [35]. Hruda et al. reported R2_{= 0.22 and R}2_{= 0.18 (both P < 0.05)}

between changes in leg extensor power and, respectively, changes in 8-ft up-and-go and 6-minute walk time in 18 healthy old adults age 85 [50]. Granacher et al. found a non-significant association of R2_{= 0.04 between changes in plantarflexor strength and gait}

velocity as a result of an 8-week-long strength and balance intervention performed in 17 healthy adults age 56 [51]. Overall, improvements in leg strength accounted for 23% of the variation in old adults’ improved gait speed.

To pinpoint the role of individual muscles, we identified 20 studies and extracted data for changes in maximal voluntary quadriceps strength and gait velocity. The twenty studies represent a total of 815 subjects with a mean age of 72, which we think fully captures the relation between quadriceps strength and improvements in gait speed in old adults. On the average, there were 30 subjects per study who exercised for 18 weeks. Gait speed was assessed over an average distance of 22 meter or timed over 5.5 min. Initial and final gait speed was 1.25 (range 0.45–2.01) and 1.38 (0.49–2.35) m/s, a

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12% increase. Mean quadriceps strength was 134 (10–423) at baseline and improved 22% to 171 (8–753) Nm after interventions. Based on the data in these 20 studies, Fig. 2.3A shows an association of R2_{= 0.21 (P < 0.018) between the changes in quadriceps}

torque and gait speed (Table A.2).

Because the largest declines occur in plantarflexor compared with knee and hip joint powers during gait (Fig. 2.1), we identified studies that measured the changes in maximal plantarflexor 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 intervention. Fig. 2.3B shows an association of R2_{= 0.16 (P = 0.432) between the changes in strength and}

gait speed in the 6 studies (Table A.2).

Figure 2.3. Associations between changes in gait

velocity and changes in leg strength or power based on studies in the literature. Panel A: Association between changes in maximal voluntary quadriceps knee extension torque and gait speed measured on a level surface in 20 studies. There are 26 data points in the graph because a few studies reported multiple measures of muscle strength or gait speed. The association is characterized by y = 063x + 14.3 and R2_{= 0.21 (P < 0.018). Panel B:} Association between changes in maximal voluntary plantarflexor torque and changes in gait velocity measured on level surface in 6 studies. There are 12 data points in the graph because several studies reported multiple measures of muscle strength or gait speed. The association is characterized by y = 0.58x + 13.8 and R2_{= 0.16 (P = 0.421).} Panel C: Association between changes in maximal voluntary leg power and changes in gait velocity measured on level surface in 8 studies. There are 9 data points in the graph because 1 study reported multiple measures of leg power or gait speed. The association is characterized by y = 0.02x + 34.6 and R2_{= 0.00 (P = 0.996). The removal} of the extreme value at the right does not affect the association. Table A.2 lists the source data and references used to construct the graphs in panels A, B, and C. ∆ Quadr iceps strenght (%) ∆ Plantarflexior strength (%) ∆ Leg po w er (%) ∆ Gait velocity (%) 40 60 20 20 40 60 80 10 20 30 40 50 10 20 30 40 50 60 80 40 60 20 80 30 40 10 0 20 50 A B C

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Considering the increasing emphasis on power vs. strength training to improve function and gait speed in old adults [52], we have identified 8 studies that measured leg power and gait speed before and after power training, representing 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. 2.3C 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 A.2). 2.5. 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 [4,49,53]. 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 plasticity of gait and candidate mechanisms of how strength interventions improve gait speed.

2.5.1. The role of relative effort

When young and old adults walk at a speed of 1.5 m/s in a laboratory, the mechanical power output of muscles supporting the body and then driving the leg from stance to swing becomes reorganized with age: the locus of function shifts to the proximal hip muscles from the distal ankle muscles (Fig. 2.1). The reduction in ankle muscle mechanical output can reach as much as 27% [33] with a 12% reduction still present even if old compared with young adults walk 13% faster [24].

Expressing leg mechanical output recorded during gait in relation to the maximal available effort allows us to operationalize mechanical plasticity of gait. The idea is that the reduced ankle function seen in old adults’ gait is associated with a reduction in maximal voluntary torque generation. There is strong evidence for a preferential decline in structure and function of nerves and muscles of lower compared with upper extremity due to age (for a review see [33]). However, the reductions in hip and knee muscle strength compared with the ankle plantarflexors strength were similar in men age 75. In addition, ankle plantarflexors compared with hip extensors were only 8% weaker in women age 73 [54]. Therefore, the distal vs. proximal weakness within the lower extremity may be less robust than the differences between upper and lower extremities. Still, using these limited data, Fig. 2.4 shows for the first time the relative effort during gait, i.e., the level of effort used at the hip, knee, and ankle joints as a percent of the

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maximal torque available at the same joints (cf. also [55]). Because maximal torque loss is similar in hip, knee, and ankle extensors [54], the torques generated during gait are the primary determinants of relative effort. The relative effort is the highest at the ankle; the above-maximal level is probably 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 [23,24,26,33,38,39,42] and the one study reporting the isokinetic data [54]. 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 [33]. Mechanical 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 expectation 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 provide virtually no evidence for either element of this expectation. First, about 80% of interventions explicitly target the knee extensors even though, as this review has uncovered it (Fig. 2.1), the age-related changes in knee kinetics are minimal vis-à-vis the 20–40% reductions in maximal voluntary knee extension torque [54,56]. As of now, no interventions have specifically targeted the ankle plantarflexors, which operate at the highest relative effort (Fig. 2.4), and linked such changes in strength to changes in ankle kinetics in the same subjects. Second, the overall consensus from the 34 studies included in our analysis is that strength and especially power gains are weakly or not at all associated with changes in gait speed (Fig. 2.3), joint kinematics, and kinetics. Although these interventions improve neuromuscular function

Young Old 140 120 100 80 60 40 20 0 Rela ti ve effor t (%) Knee Ankle Hip

Figure 2.4. 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. 2.1 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.

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25% and old adults walk 11% faster, the evidence is weak that old adults walk faster because they use the newly acquired physical abilities in gait (Tables A.1 and A.2 in Appendix A). 2.5.2. 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. 2.5 provides one model that considers a successful incorporation of newly acquired strength into gait (Fig. 2.5A) and shows another model that predicts an increase in gait speed with little or no incorporation of newly acquired muscle strength (Fig. 2.5B). To date, there is no gait kinetics data to verify the incorporation model (Fig. 2.5A). The little biomechanical data available show an inconsistent picture. Kinematic analysis revealed a key role for knee function [35], whereas mechanical energy expenditure analysis showed a decreased role for knee function in gait speed adaptations [47]. Even within the same study, the pattern of association between changes in strength and function was inconsistent: improved plantarflexion and hip function (6° more flexion) was marginally associated (R2_{= 0.17,}

P = 0.049) with gait speed but changes in knee function and gait speed correlated R2₌

0.44 (P = 0.001) [35]. The 6° more hip flexion is in line with predictions by mechanical plasticity (i.e., a shift of function to hip from the ankle) but then these changes poorly correlated with gait speed. On the other hand, mechanical plasticity predicts not much need for a change at the knee (due to its low relative effort), yet increases in quadriceps strength correlated strongest with changes in gait speed (R2_{= 0.44, P =}

0.001). This last piece of data provides perhaps the first still somewhat unconvincing hint that old adults may be able to incorporate a small portion of the newly acquired voluntary strength into knee function and causing changes in gait speed. Puzzlingly, a composite exercise program improved muscle strength 14% and produced kinematic adaptations at the hip, knee, and ankle joints. However, the larger range of motions, and presumably accelerations, at these joints did not increase gait speed (4%, n.s.) [48]. Thus, an intervention can modify gait biomechanics without a putative increase in gait speed.

Although conceptually and empirically functional performance, including gait speed, is associated with leg power ~R2_{= 0.50 [52,57–59] and modeling studies show}

increased gait speed with increased muscle power [60–64], our finding that improvements in leg power had R2_{= 0.00 association with improvements in gait speed was unexpected}

(Fig. 2.3C, Table A.2). We interpret these data to mean that mechanism of adaptation in gait speed in response to power training is unknown and not understood. An extensive analysis of adaptations to strength and power training in a previous review [4] provides a perspective for our finding of this low association between changes in gait speed and changes in leg power. The idea is that perhaps the changes in gait speed and leg power association would become

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much stronger if future studies followed more closely the exercise specificity principle by having old adults exercise at low intensities (20–40% of maximum power) improving both gait speed and leg power [65]. However, the mechanism is very likely multi-factorial and interactive between biomechanical, physiological, neurological and psychological factors.

Anyone will increase walking speed by generating more muscle force and power but the current biomechanical data do not bear out this mechanism. Fig. 2.5B describes a situation in which old adults operate close to maximum effort pre-training. Training increases maximum effort and adults now walk with more force than they previously had but not much more force and still below the pretraining maximum. Old adults operating closer to their performance limits [55] (Fig. 2.4) may not as well incorporate newly acquired maximal strength into locomotor tasks: they adopt strategies that allow them to use so far unexploited resources more effectively. We speculate that perhaps they use new and previously non-existent levels of muscle force and power. They may increase the use of force to levels that were already available before the intervention but for some reason were unused. In particular, it seems an equally reasonable and untested possibility that interventions improve gait speed because old adults simply feel more comfortable after the intervention as they operate at a lower effort relative to their

Figure 2.5. Conceptual models of how strength and

power training interventions 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 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 previously had yet with lower effort relative to their maximal ability. Maximal ability (open column) is quantified by joint torques measured through inverse dynamics 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 filled column in post- compared to pre-test. There is currently no evidence for the incorporation model. B: Similar to the Model in A, old adults walked (filled column) just below their maximal ability (open column) pre-training. The narrow difference 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 previously had but not much more force, denoted by the small difference between the two filled columns pre- and post-training. That is, the relative effort decreased less in Model B than in Model A. However, the effort needed to walk (filled column in post-test) is still below the pre-training maximum (open column in pre-test). This model predicts little incorporation of newly acquired strength into gait. There is indirect biomechanical evidence for this model. Ultimately, either mechanism still must act through the final common pathway of higher muscle force generation that increases kinetic energy and gait speed. Walking ability Maximal ability A B 100 80 60 40 20 0 Effor t (arbitrar y unit) 100 80 60 40 20 0 Effor t (arbitrar y unit) Pre Post

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maximal capabilities and exploit already existing physiological resources and not because the new levels of strength or power increases the mechanical output of the ankle, knee, and hip joint muscles. Interventions may also increase gait speed by improving the coordination between pairs of agonist and antagonist muscles which in turn could reduce the metabolic cost of transport and the relative effort [36,66,67] and through an optimization of irregular and variable gait [68–70]. Perhaps the mechanism acts through improved psychological, “strength,” i.e., self-efficacy, less resistance to rotate joints through the range of motion, or a motor unit effect in which even if maximum strength is not increased, motor units are more readily activated. Recent theories suggest that exercise may indeed reduce the rate of falls through its beneficial effects on cognitive function in old adults [71]. There are also profound age-related changes in tendon properties, including a reduction in stiffness that can be modified by exercise training [72,73]. Still, each and any of these mechanisms must act through the final common pathway of higher muscle force generation that increases kinetic energy and gait speed.

Finally, we note that virtually any type of intervention even those not designed explicitly to improve muscle strength and power can increase gait speed. Walking speed increased following balance, endurance, functional [74], combination [48,75], walking training with [76] and without [77] body weight unloading, and Tai Chi exercise [78] (for a review see [4,22,79]. Any and all of the interventions clinicians currently prescribe for old adults can improve neuromuscular function and perhaps the increased gait speed is a secondary but Valuable outcome as are improvements in balance and sit-to-stand. This generalized effects of interventions may be related to the idea that functional improvements after an intervention dot not scale to a dose–response relationship because the stimulus for increasing gait speed is different in magnitude and nature than the exercise dose that improves maximal voluntary force and power (cf. [22]). That is, the stimulus to increase gait speed is lower in magnitude than the stimulus for strength gains so that training with high loads elicits a response at lower level activities. After training old adults become stronger and operate at lower relative levels of their maximal capacities and thus more comfortable absolute levels.

2.6. SUMMARY AND RECOMMENDATIONS

Clinicians routinely prescribe strength and power interventions for old adults in an effort to improve ADL mobility, including gait speed [21,52]. The present review shows that the biomechanical mechanisms of how, if at all, the intervention-improved physical capacity becomes incorporated into the movements of ADLs and in case of gait, produces faster walking, is not known. An analysis of over 30 studies revealed that the association between improvements in leg muscle strength and gait speed is R2_{= 0.21}

and between the changes in leg power and changes in gait speed is R2_{= 0.00. To increase}

the efficacy of intervention studies designed to improve gait speed and other critical mobility functions in old adults, there is a need for a paradigm shift from conventional

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outcome assessments to more sophisticated biomechanical analyses that examine joint kinematics, kinetics, energetics, muscle–tendon function, and musculoskeletal modeling before and after interventions. Physiological, neurological, and psychological tests could enhance the biomechanical studies and identify the full spectrum of exercise-induced modifications in walking performance.

We recommend that future studies perform whole body kinematic and kinetic analyses of gait before and after strength and power training that targets hip, knee, and ankle muscles individually and in combination. The gait tests should be performed at a self-selected pace and also at a fixed speed to identify adaptations due to intervention and also due to age. The goal is to determine if strength and power interventions that increase maximal voluntary torque also increase lower extremity joint torques and powers and if these changes are associated with changes in critical properties of gait such as step length and gait speed. Many studies use composite interventions comprising 4–6 elements with clear intentions to improve multiple aspects of mobility. However, it is not possible to determine which specific element or an interaction between the elements cause the biomechanical, physiological, and motor control adaptations in gait. There is a need to systematically examine the effects of individually tailored interventions on the association between changes in gait mechanics and neuromuscular outcomes. Although this review focused on leg muscle function, the possibility exists that interventions also affect trunk behavior, which, in a proximal to distal direction, can affect the biomechanics of leg muscles, hence gait speed. Studies are needed to determine if interventions modify not only horizontal but also vertical kinematics of gait as such measures directly reflect muscle work, hence metabolic and mechanical cost of gait. Future studies should determine if age uniformly affects hip, knee, and ankle muscles within the same individuals. Such data would allow clinicians to more effectively personalize intervention targets and determine if interventions reduce relative effort during gait, which we propose as a critical marker of mobility and disability in old adults.

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