Deficient limb support is a major contributor to age differences in falling

Deficient limb support is a major contributor to age differences in falling

ARTICLE IN PRESS Journal of Biomechanics 40 (2007) 1318–1325 www.elsevier.com/locate/jbiomech www.JBiomech.com Deficient limb support is a major cont...

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ARTICLE IN PRESS

Journal of Biomechanics 40 (2007) 1318–1325 www.elsevier.com/locate/jbiomech www.JBiomech.com

Deficient limb support is a major contributor to age differences in falling Michael J. Pavola, Yi-Chung Paib, a

Department of Nutrition and Exercise Sciences, Oregon State University, Corvallis, OR 97331, USA Departments of Physical Therapy, Movement Sciences, Bioengineering, and Mechanical and Industrial Engineering, University of Illinois at Chicago, 1919 W. Taylor Street, 4th Floor, Chicago, IL 60612, USA

b

Accepted 17 May 2006

Abstract Older adults are more likely than young to fall upon a loss of balance, yet the factors responsible for this difference are not well understood. This study investigated whether age-related differences in movement stability, limb support, and protective stepping contribute to the greater likelihood of falling among older adults. Sixty young and 41 older, safety-harnessed, healthy adults were exposed to a novel and unexpected forward slip during a sit-to-stand task. More older than young adults fell (76% vs. 30%). Falls in both age groups were related to lesser stability and lower hip height at first step touchdown, with 97.1% of slip outcomes correctly classified based on these variables. Decreases in hip height at touchdown had over 20 times greater effect on the odds of falling than equivalent decreases in stability. Three age differences placed older adults at greater risk of falling: older adults had lower and more slowly rising hips at slip onset, they were less likely to respond to slipping with ample limb support, and they placed their stepping foot less posterior to their center of mass. The first two differences, each associated with deficient limb support, reduced hip ascent and increased hip descent. The third difference resulted in lesser stability at step touchdown. These results suggest that deficient limb support in normal movement patterns and in the reactive response to a perturbation is a major contributor to the high incidence of falls in older adults. Improving proactive and reactive limb support should be a focus of fall prevention efforts. r 2006 Elsevier Ltd. All rights reserved. Keywords: Older adults; Slips; Stability; Limb collapse

1. Introduction Falls are a serious and growing health concern for older adults (Kannus et al., 1999). Their consequences include fear-related restriction of activities, serious injury, and even death (National Safety Council, 2004; Stel et al., 2004; Tinetti et al., 1988). Increased fall risk in older adults has been attributed to a variety of sensory, motor, cognitive, environmental, and medical factors (Moreland et al., 2003; Myers et al., 1996; Northridge et al., 1995). In particular, many aging-related changes in the postural Corresponding author. Tel.: +1 312 996 1507; fax: +1 312 996 4583. E-mail address: [email protected] (Y.-C. Pai).

0021-9290/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2006.05.016

and stepping responses used to maintain and regain balance have been identified (Maki and McIlroy, 1996; McIlroy and Maki, 1996; Mille et al., 2003; Stelmach et al., 1989). However, the mechanisms whereby older adults actually fall following a loss of balance have been little investigated (Lockhart et al., 2003; Pavol et al., 2001; Pijnappels et al., 2005). Arguably, understanding these mechanisms will allow for more effective intervention against falls by older adults. Factors that can play large roles in falling are movement stability, hip vertical motion related to limb support of body weight, and protective stepping for balance recovery (Pavol et al., 2004a). Instability, representing an inability to regulate or terminate the horizontal motion of the body center of mass (COM)

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over the base of support, will lead to a fall unless stability is reestablished through a change in base of support, typically by protective stepping. For a backward balance loss, this requires a step of sufficient length to place the stepping foot posterior to the COM. By normal definition, however, falls result from vertical descent of the body. Such descent will result from instability and/or from insufficient limb support. Of particular concern is the potential, during stepping, for the single support limb to collapse under the body’s weight (Pai et al., in press). Decreases in hip height increase the required stepping knee flexion. Thus, excessive hip descent prior to step touchdown might restrict step length due to reduced clearance or result in a highly flexed limb configuration at touchdown, making the limb unable to arrest the body’s descent; a fall could result despite improved stability. In theory, lesser stability and lower hip height at step touchdown should be highly predictive of falls. These may, in turn, be related to stability and hip height at perturbation onset. Indeed, falls by young adults following a slip during a sit-to-stand movement were attributable to lesser stability at slip onset, followed by a shortened backward step and simultaneous limb collapse (Pavol et al., 2004a). Recent experiments confirmed that healthy older adults are more likely than young to fall upon experiencing a novel, unexpected perturbation during movement, specifically a slip during a sit-to-stand (Pavol et al., 2002b). The factors responsible for this difference are not well understood, however. This study therefore investigated whether age-related differences from slip onset through step touchdown in movement stability, in hip vertical motion related to limb support, and in protective stepping explained the greater likelihood of falling among older adults.

2. Methods The subjects and protocol have been detailed previously (Pavol et al., 2002b). Forty-one healthy, community-dwelling older adults (mean7SD age: 7375 years (range: 65–85); height: 1.6970.09 m; mass: 79714 kg; 21 women) and 60 healthy young adults (age: 2575 years; height: 1.6970.10 m; mass: 67714 kg; 44 women) gave written informed consent to participate. Subjects were screened for neurological, musculoskeletal, cardiopulmonary, and other systemic disorders. Older adults were further screened for cognitive impairment (Folstein et al., 1975), poor mobility (Podsiadlo and Richardson, 1991), orthostatic hypotension, and bone loss (i.e. osteopenia or osteoporosis). Institutional review board approval was obtained.

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2.1. Experimental protocol A novel, unexpected slip was induced during a sit-tostand movement using a side-by-side pair of low-friction platforms (dimensions: 31  29  2.5 cm; friction coefficient: 0.02; Fig. 1). These were free to slide 24 cm forward upon release of their locking mechanisms. Platforms slid independently and latched into place in their maximum forward positions. Subjects wore a fullbody safety harness, attached from the shoulders to a ceiling-mounted support by a pair of shock-absorbing ropes. A load cell measured the force exerted on the ropes. Trials began with subjects sitting on a stool in a standardized position: one shoe on each platform, ankles dorsiflexed 101, knees flexed 801, arms at the sides, and elbows flexed 901. Subjects were told that they would initially be performing sit-to-stand trials and that, ‘‘later on,’’ a slip would take place. No practice or instructions regarding the slip were given, nor were the trial, timing, or mechanisms of the slip provided. Subjects were to stand up ‘‘as quickly as possible,’’ without using their arms, then remain standing still. After four normal sit-to-stand trials, a slip was induced without warning. A computer triggered the slip, releasing both platforms when the stool supported less than 10% body weight and the forward velocity of the body COM exceeded 20 cm/s. The slip was thereby initiated 16711 ms after seat-off. Slip initiation was controlled

load cell safety harness

5% body ht.

fall criterion height

stool 24cm

force plates

sliding platforms

Fig. 1. Diagram of the experimental setup. The average body position of the older adults at slip onset is shown. The safety harness system is not to scale; its upper anchor was 3.2 m above the floor. Dotted gray lines indicate the leg and thigh configuration in the initial seated position. A fall resulted if the midpoint between the computed hip joint centers descended below the illustrated criterion height.

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by real time data from three force plates (AMTI, Newton, MA) located beneath the stool and each platform. The COM velocity was determined from the time integral of the shear forces. The coordinates of 26 markers attached to the bilateral upper and lower extremities, torso, and platforms were recorded by a motion capture system at 60 Hz (Vicon Peak, Centennial, CO). Marker paths were later low-pass filtered at marker-specific cut-off frequencies (range: 4.5–9 Hz) using recursive, fourth-order Butterworth filters. Force plate and safety harness data were collected at 600 Hz. 2.2. Data analysis Positions of joint centers, heels, and toes in threedimensional space were computed from the filtered marker paths using transformations derived from anthropometric measurements. The position of the body COM was computed using sex- and age-dependent inertial parameters (de Leva, 1996; Pavol et al., 2002a) in a 13-segment kinematic model with separate pelvis, torso, and head segments. Slip outcomes were classified as falls if the midpoint between the calculated hip joint centers descended within 5% body height of its initial seated height (Pavol et al., 2002b). Recoveries occurred if the average force on the safety harness did not exceed 4.5% body weight over any 1-s period. The remaining outcomes were considered harness affected. Movement stability and hip vertical motion were determined at or between six events of interest for each slip. From visual inspection, slip onset was 16 ms before the displacement of either platform from its initial position exceeded three SD of the measurement noise. Mid-slip occurred when the forward displacement of the more posterior platform reached 12 cm. The start of hip descent corresponded to the first downward motion of the hip midpoint. Step initiation corresponded to the start of a simultaneous decrease in vertical force beneath the stepping foot and increase beneath the support foot that continued until step lift-off. Step lift-off and step touchdown were determined from the absence or presence of force on the force plates. Movement stability was computed from the COM’s state (i.e. instantaneous position and velocity). The COM anterior position and forward velocity were found relative to the heel and support surface of the posterior foot in ground contact, p respectively. They were normalffiffiffiffiffiffiffiffiffiffiffiffi ized by foot length and g  bh, respectively, where g is the acceleration due to gravity and bh is body height (McMahon, 1984). Threshold boundaries have previously been derived within the COM state space for backward balance loss on a nonslip or a frictionless surface (Pai and Iqbal, 1999). Outside a given boundary, balance recovery is theoretically impossible under the

corresponding conditions without a change in base of support. Stability was quantified as the shortest inwardly directed distance from the applicable boundary to the instantaneous COM state (Pai et al., 2003). Before step touchdown, the boundary for backward balance loss on a frictionless surface applied. At step touchdown, the boundary for a nonslip surface was used instead for the 87% of slips in which touchdown was on a stationary surface. Hip vertical motion related to limb support was quantified by the height and upward velocity of the hip midpoint relative to the support surface. Hip variables were normalized by body height. Where stepping occurred, the length of the initial step was computed as the posterior-directed position of the stepping ankle relative to the support ankle at step touchdown. Steps where lift-off occurred after the time of fall were excluded (Pavol et al., 2002b). 2.3. Statistics Fisher’s exact test identified age differences in the distributions of falls and recoveries, of falls with and without stepping, and of recoveries with one and multiple backward steps. Four young adults were excluded from analysis due to lost data or equipment malfunction. Four recoveries and one fall by young adults and one recovery and one fall by older adults were atypical and not analyzed further. Univariate logistic regressions determined the influence, across all subjects, of each kinematic variable on the odds of falling. No-step falls by young adults were excluded from further analysis, due to their low incidence. Two-factor analyses of variance (ANOVA), with Bonferroni-corrected post hoc t-tests, identified kinematic differences between slip outcome and age groups among subjects who stepped. Among older adults, ANOVA identified differences between those who recovered, fallers who stepped, and no-step fallers, with the Dunnett test used for post hoc comparison to the no-step fallers. Forward, stepwise logistic regression determined the influence of stability at step touchdown, hip height at touchdown, and age group on the likelihood of falling. The likelihood ratio test with a cutoff probability of 0.05 was used for variable entry, with a threshold probability of 0.5 used for classification. A significance level of 0.05 was used throughout. Analyses were performed using SPSS 12.0 (Chicago, IL).

3. Results A greater proportion of older than young adults fell upon the novel, unexpected slip (po0:001; Table 1). Excluding harness-affected outcomes, 76% of older

ARTICLE IN PRESS M.J. Pavol, Y.-C. Pai / Journal of Biomechanics 40 (2007) 1318–1325 Table 1 Outcomes of the slips induced in young and older adults

Slip Onset

0.1

Backward steps

Recover

0 1 X2 Total

1 22 12a 35

0 1 8 9

0 1 X2 Total

3 9 3 15

11b 14 4 29

Total

6

3

Harness affected

Older (n ¼ 41)

Occurrences are shown according to age group and the number of backward steps completed (i.e. stepping ankle posterior to the contralateral ankle at step touchdown) either during the recovery or prior to the time of the fall. a Includes two subjects whose first step was not backward. b Includes one subject who completed a forward step.

adults fell versus 30% of young. While all but one recovery included a protective step, 30% of fallers did not step, regardless of age group (p ¼ 0:52). Slipping produced instability, necessitating a backward step for recovery (Fig. 2); those who did not step fell. Although young fallers were less stable than all others at slip onset, this difference disappeared by midslip, such that stability at or before mid-slip was unrelated to the odds of falling (Table 2). Among those who stepped, falls were related to lesser stability at step touchdown (Table 2). Fallers, regardless of age, took a shorter backward step and placed their stepping foot less posterior to their COM than those who recovered (Table 3). Older adults, regardless of outcome, placed their stepping foot less posterior to their COM than the young (on a stationary surface in all but one case), resulting in lesser stability at step touchdown. Consistent with this, older adults were more likely to employ a second backward step for successful recovery (p ¼ 0:006; Table 1). In both young and older adults, falls were most strongly related to deficient limb support (Table 4; Fig. 3). To start, lower hip heights and slower upward hip velocities at slip onset were associated with greater odds of falling. These characteristics, although absent in young fallers, were exhibited by older adults regardless of outcome. Everyone then experienced hip descent starting 180–750 ms after slip onset. Lower hip heights at the start of descent increased the odds of falling. In particular, the hips of older fallers started to descend from lower heights than in all others. Regardless of age, fallers then exhibited greater hip descent between step initiation and touchdown, leading to lower hip heights at step touchdown. Hip height at step touchdown was

Step TD

COM velocity / g . bh

Slip outcome

Fall

Young (n ¼ 56)

1321

0

-0.1 Young:Recover Young:Fall:Step

-0.2

Older:Recover Older:Fall:Step Mid-Slip Older:Fall:No-Step

-0.3 -0.5

-0.25

0

0.25

0.5

0.75

COM position / foot length

Fig. 2. State-space diagram of the anteroposterior postion and velocity of the body center of mass (COM) relative to the base of support at slip onset, mid-slip, and step touchdown (TD). Mean7SD values at each event are shown as a function of age group, slip outcome, and the presence or absence of a stepping response. COM anterior position and forward velocity are expressed relative to the heel position and support surface velocity, respectively, of the posterior foot in ground contact. pffiffiffiffiffiffiffiffiffiffiffi ffi Positions and velocities are normalized to foot length and g  bh, respectively (g ¼ acceleration due to gravity; bh ¼ body height). Also shown are the model-predicted threshold boundaries for backward balance loss on a nonslip surface (dotted gray line) or on a frictionless surface (solid gray line; Pai and Iqbal, 1999). The regions marked in gray and with diagonal lines comprise those COM states that are stable under nonslip and slipping conditions, respectively (i.e. anteroposterior movement may be terminated without a backward step). Stability was quantified as the shortest inwardly directed distance from the applicable boundary to the instantaneous COM state. Ellipses group the symbols corresponding to the same event.

the strongest predictor of slip outcome; a decrease of one SD ( ¼ 3.6% body height across subjects) increased the odds of falling by a factor of 102. Lesser stability at step touchdown also increased the likelihood of falling due to a lower hip height at touchdown. A logistic model with these two variables correctly classified 97.1% of slip outcomes after a protective step (Fig. 4). Age group did not enter into the model. Fallers were classified with both a sensitivity and a specificity of 97%. Finally, no measure of stability or hip height from slip onset through mid-slip and the start of descent differed between older fallers who did and did not step (Tables 2 and 4).

4. Discussion This study has elucidated the complex roles of movement stability, limb support, and protective stepping in falls by young and older adults following a

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Table 2 Mean7SD kinematics of anteroposterior stability (  102) as a function of age group, slip outcome, the presence or absence of a protective stepping response, and as related to the odds of falling Event

Slip onset Mid-slipd Step touchdown

Young

Older

Recover (n ¼ 31)

Fall:step (n ¼ 11)

Fall:no-step (n ¼ 3)b

Recover (n ¼ 8)

Fall:step (n ¼ 18)

Fall:no-step (n ¼ 10)

8.974.1 14.679.7e 7.578.6f

4.574.7c 20.176.1e 0.879.3f,g

3.176.0 20.374.7 —

9.474.7 25.378.3 0.675.5

11.674.5 21.477.8 4.775.2g

13.075.0 18.775.6 —

Odds ratio for fallinga 0.92 1.49 4.55h

Stability ¼ distance of COM state from model-predicted boundary for backward balance loss (o0 indicates unstable). a Factor by which the odds of falling change for a decrease of 1 SD in the variable across all subjects. b Not included in the statistical analyses. c po0:05 vs. young recover and older fall:step (interaction of age group and slip outcome). d Excludes nine young recover, four young fall:step, and one older recover subjects who stepped before the posterior foot reached the slip midpoint. e po0:05 vs. older (main effect of age group). f po0:01 vs. older (main effect of age group). g po0:01 vs. recover (main effect of slip outcome). h po0:001 for odds ratio6¼1. Table 3 Mean7SD kinematics of the first protective step as a function of age group, slip outcome, and as related to the odds of falling Variable

Step length (%bh) XCOM at step TD (% ft len)

Young

Older

Recover (n ¼ 31)

Fall:step (n ¼ 11)

Recover (n ¼ 8)

Fall:step (n ¼ 18)

12.576.5 39.0723.8d

10.676.6b 6.5731.5d,e

11.974.8 20.7721.1

5.674.0b 15.3727.8e

Odds ratio for fallinga 2.36c 6.67f

XCOM ¼ center of mass anteriorly directed position relative to heel of stepping foot; TD ¼ touchdown; bh ¼ body height; ft len ¼ foot length. a Factor by which the odds of falling change for a decrease of 1 SD in the variable across all subjects. b po0:05 vs. recover (main effect of slip outcome). c po0:01 for odds ratio6¼1. d po0:01 vs. older (main effect of age group). e po0:001 vs. recover (main effect of slip outcome). f po0:001 for odds ratio6¼1. Table 4 Mean7SD kinematics of limb support as a function of age group, slip outcome, the presence or absence of a protective stepping response, and as related to the odds of falling Variable

ZHIP at slip onset (%bh) dZHIP/dt at slip onset (%bh/s) ZHIP at hip descent (%bh) DZHIP, step init to TDh (%bh) ZHIP at step TD (%bh)

Young

Older

Recover (n ¼ 31)

Fall:step (n ¼ 11)

Fall:no-step (n ¼ 3)b

Recover (n ¼ 8)

Fall:step (n ¼ 18)

Fall:no-step (n ¼ 10)

43.971.5c 37.178.2c 52.171.4 1.271.6c 50.771.6

43.671.7c 38.078.3c 51.171.8 5.872.6c,i 45.072.3i

43.171.9 40.375.3 51.270.9 — —

42.870.8 28.476.0 51.371.0 0.371.7 50.471.1

41.871.7 23.175.3 47.972.2e 3.171.9i 44.172.6i

42.471.6 23.274.8 47.972.2f — —

Odds ratio for fallinga 2.17d 2.27d 7.14g 7.69g 101.95g

ZHIP ¼ height of hip midpoint; dZHIP/dt ¼ upward vertical velocity of hip midpoint; hip descent ¼ start of hip descent; step init ¼ step initiation; TD ¼ touchdown; bh ¼ body height; D ¼ change. a Factor by which the odds of falling change for a decrease of 1 SD in the variable across all subjects. b Not included in the statistical analyses. c pp0:001 vs. older (main effect of age group). d po0:01 for odds ratio6¼1. e po0:001 vs. young fall:step and older recover (interaction of age group and slip outcome). f po0:01 vs. older recover (not compared to young). g po0:001 for odds ratio6¼1. h Step initiation could not be identified in one young recover, one young fall:step, and three older fall:step subjects. i po0:001 vs. recover (main effect of slip outcome).

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55 Start of Hip Descent

ZHIP (%bh)

50 Step TD

Slip Onset

45 Young:Recover Young:Fall:Step

40

Older:Recover Older:Fall:Step Older:Fall:No-Step

35 0

0.1

0.2 0.3 0.4 Time after Slip Onset (s)

0.5

0.6

Fig. 3. Hip height (ZHIP) kinematics at slip onset, the start of hip descent, and step touchdown (TD), showing the timing of each event relative to slip onset. Mean7SD values are shown as a function of age group, slip outcome, and the presence or absence of a stepping response. Hip height, from the support surface to the midpoint between the calculated hip joint centers, was normalized to body height (bh). The data at slip onset (i.e. 0 s) have been offset in time for display purposes. Boxes group the symbols corresponding to the same event.

55

ZHIP at Step TD (%bh)

53 51 49 47 45

Young:Recover

43

Young:Fall Older:Recover

41

Older:Fall

39 -0.3

-0.2

-0.1

0 0.1 0.2 Stability at Step TD

0.3

0.4

Fig. 4. Relationship between anteroposterior stability at touchdown of the first protective step, the corresponding height of the hip midpoint (ZHIP, in %bh; bh ¼ body height) at step touchdown, and the outcome of the induced slip in young and older adults. Individuals within the shaded region would be classified as likely to fall by the derived logistic regression model: p(fall) ¼ 1/(1+exp(69.18+18.36 stability +1.454ZHIP)) (po0.05 for all model coefficients). The logistic model correctly classified 97% of slip outcomes.

novel, unexpected slip. Regardless of age, recovery from a backward balance loss depended on executing a stepping response that provided adequate stability and hip height at step touchdown. Slipping induced instability, and individuals who did not respond by stepping fell. Among those who stepped, fallers placed their stepping foot less posterior to the COM, resulting in lesser stability at step touchdown. Simultaneously, fallers exhibited greater collapse of the support limb due

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to deficient limb support while stepping, as evidenced by greater hip descent that resulted in lower hip heights at step touchdown. Jointly, stability and hip height at step touchdown were highly predictive of falling, explaining 97% of outcomes. Of these variables, hip height was the primary determinant of slip outcome, with decreases increasing the odds of falling 22 times more than an equivalent decrease in stability. Stability and hip height at step touchdown were also directly related (r ¼ 0:49; po0:001). Avoiding a fall thus vitally depended on providing sufficient limb support to limit hip descent, thereby facilitating an effective step to re-establish stability. This further supports the critical role of the support limb in protective stepping (Pai, 1999; Pavol et al., 2001, 2004a; Pijnappels et al., 2004). Stability at step touchdown was less critical. Of eight older adults analyzed who recovered, five were actually unstable at step touchdown. But because they limited their hip descent, their instability could be resolved by stepping again. All eight took a second step backward, consistent with past observations of increased multiple stepping by older adults during balance recovery (Luchies et al., 1994; McIlroy and Maki, 1996). Older adults were 2.5 times more likely than young to fall due to three apparent factors. First, older and young adults differed in their execution of the sit-to-stand task, such that the hips of older adults were lower and rising more slowly at slip onset. Second, older adults were less likely than young to respond to the slip with ample limb support. Fallers, independent of age, did less knee extensor work for support from seat-off through step touchdown (Pai et al., in press). As a combined result, the 76% of older adults who fell achieved lesser hip height than the young before starting to descend, and those who stepped experienced substantial collapse of the support limb (evidenced by hip descent) following step initiation. These led to low hip heights at step touchdown. Third, older adults placed their stepping foot less posterior to their COM, resulting in lesser stability at step touchdown, or they failed to step entirely. Together, the low hip height and instability made it impossible to recover without stepping again and impossible to take such a step. Notably, 28% of older adults failed to step, versus only 6% of young. Older fallers who did not step differed from those who did only in their absence of a stepping response. Thus, had they stepped, the older nostep fallers would likely still have fallen due to their low hip height at the start of descent. Instead, these fallers appeared to employ a squatting/sitting response (Pavol et al., 2002b). Such a response is an effective strategy for reducing the body’s energy at landing impact (Robinovitch et al., 2004; Sandler and Robinovitch, 2001). Arguably, the older no-step fallers’ deficient limb support led them to suppress stepping, under the

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prediction that it would fail, and attempt to land safely instead. The factors that placed older adults at greater risk of falling could reflect differences in muscle strength, neuromuscular control, or both. Slower ascent during a sit-to-stand is characteristic of older adults (Pai et al., 1994) and has been associated with decreased strength (Corrigan and Bohannon, 2001; Schot et al., 2003). However, the deficient limb support after slip onset in the present fallers was likely not from lack of strength. With one possible exception, all fallers possessed sufficient strength to recover upon subsequent exposure to the perturbation (Pavol et al., 2002b). Also, hip ascent at slip onset did not differ between older adults who recovered and those who fell, implying that they were similar in strength. The deficient limb support of the fallers after slip onset was therefore likely attributable to their poor initial reactive responses. A spectrum of reflex and triggered responses exists within and across limbs, and these responses are influenced by the ‘‘postural set’’ inherent to supraspinal modulation or control (Horak and Nashner, 1986; Horak et al., 1989). The deficient limb support of the fallers may reflect a ‘‘postural set’’ that was biased, from lack of experience and/or readiness, toward an ineffective response. Because the knee extension needed for limb support after slip onset is destabilizing during a backward loss of balance, the fallers may have responded by initially limiting their knee extension moments, as reported by Pai et al. (in press), in a failed attempt to maintain stability. This suggests that limb support is of higher priority than resisting balance loss in avoiding a fall. The present findings correspond to novel, unexpected slips by healthy older adults during a sit-to-stand; the extent to which they apply to other perturbations, populations, or tasks is unknown. The mechanical effects of different perturbations vary. Experience and expectation also alter the reactive responses to a perturbation such as to reduce the likelihood of falling (Horak et al., 1989; Pavol et al., 2004b). Thus, older adults may be less likely to respond poorly to a familiar perturbation. If true, training older adults’ reactive responses through perturbation exposures might aid in falls prevention. However, there likely exist other agingrelated differences, such as severe impairments in strength or balance among frailer older adults, that increase the likelihood of falling when perturbed. The relative importance of the factors that affect falling may also vary between tasks, particularly if hip height at perturbation onset varies. In the present results, falls by both young and older adults were most strongly associated with deficient limb support. This was primarily in the form of an ineffective reactive response that did not adequately maintain hip height after slip onset, thereby impeding the restoration

of stability by protective stepping. Older adults were far more likely than young to exhibit such a response. Older adults further exhibited deficient limb support even before slip onset, with slower ascent during the sit-tostand task. These results suggest that deficient limb support, in normal movement and in the reactive response to a novel, unexpected perturbation, is a major contributor to the high falls incidence in older adults. Improving proactive and reactive limb support should therefore be a focus of fall prevention efforts.

Acknowledgments This work was funded by NIH R01-AG16727 (YCP) and the Whitaker Foundation (YCP). The experiments were conducted in the Department of Physical Therapy and Human Movement Science at Northwestern University Medical School. The authors thank the Buehler Center on Aging, Dr. Beatrice Edwards, and Dr. Folasade Ojo for assisting in subject recruitment and screening, Eileen Runtz, Genevieve Gagnon, and Jason Wening for assisting in data collection and processing, and Dr. Feng Yang for assisting with the analysis. References Corrigan, D., Bohannon, R.W., 2001. Relationship between knee extension force and stand-up performance in community-dwelling elderly women. Archives of Physical Medicine and Rehabilitation 82, 1666–1672. de Leva, P., 1996. Adjustments to Zatsiorsky–Seluyanov’s segment inertia parameters. Journal of Biomechanics 29, 1223–1230. Folstein, M.F., Folstein, S.E., McHugh, P.R., 1975. ‘‘Mini mental state’’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 12, 189–198. Horak, F.B., Nashner, L.M., 1986. Central programming of postural movements: adaptation to altered support-surface configurations. Journal of Neurophysiology 55, 1369–1381. Horak, F.B., Diener, H.C., Nashner, L.M., 1989. Influence of central set on human postural responses. Journal of Neurophysiology 62, 841–853. Kannus, P., Parkkari, J., Koskinen, S., Niemi, S., Palvanen, M., Ja¨rvinen, M., Vuori, I., 1999. Fall-induced injuries and deaths among older adults. Journal of the American Medical Association 281, 1895–1899. Lockhart, T.E., Woldstad, J.C., Smith, J.L., 2003. Effects of agerelated gait changes on the biomechanics of slips and falls. Ergonomics 46, 1136–1160. Luchies, C.W., Alexander, N.B., Schultz, A.B., Ashton-Miller, J.A., 1994. Stepping responses of young and old adults to postural disturbances: kinematics. Journal of the American Geriatrics Society 42, 506–512. Maki, B.E., McIlroy, W.E., 1996. Postural control in the older adult. Clinics in Geriatric Medicine 12, 635–658. McIlroy, W.E., Maki, B.E., 1996. Age-related changes in compensatory stepping in response to unpredictable perturbations. Journal of Gerontology: Medical Sciences 51A, M289–M296. McMahon, T.A., 1984. Muscles, Reflexes, and Locomotion. Princeton University Press, Princeton, NJ.

ARTICLE IN PRESS M.J. Pavol, Y.-C. Pai / Journal of Biomechanics 40 (2007) 1318–1325 Mille, M.-L., Rogers, M.W., Martinez, K., Hedman, L.D., Johnson, M.E., Lord, S.R., Fitzpatrick, R.C., 2003. Thresholds for inducing protective stepping responses to external perturbations of human standing. Journal of Neurophysiology 90, 666–674. Moreland, J., Richardson, J., Chan, D.H., O’Neill, J., Bellissimo, A., Grum, R.M., Shanks, L., 2003. Evidence-based guidelines for the secondary prevention of falls in older adults. Gerontology 49, 93–116. Myers, A.H., Young, Y., Langlois, J.A., 1996. Prevention of falls in the elderly. Bone 18, 87S–101S. National Safety Council, 2004. Injury Facts. National Safety Council, Itasca, IL. Northridge, M.E., Nevitt, M.C., Kelsey, J.L., Link, B., 1995. Home hazards and falls in the elderly: the role of health and functional status. American Journal of Public Health 85, 509–515. Pai, Y.-C., 1999. Induced limb collapse in a sudden slip during termination of sit-to-stand. Journal of Biomechanics 32, 1377–1382. Pai, Y.-C., Iqbal, K., 1999. Simulated movement termination for balance recovery: can movement strategies be sought to maintain stability in the presence of slipping or forced sliding? Journal of Biomechanics 32, 779–786. Pai, Y.-C., Naughton, B.J., Chang, R.W., Rogers, M.W., 1994. Control of body centre of mass momentum during sit-to-stand among young and elderly adults. Gait and Posture 2, 109–116. Pai, Y.-C., Wening, J.D., Runtz, E.F., Iqbal, K., Pavol, M.J., 2003. Role of feedforward control of movement stability in reducing sliprelated balance loss and falls among older adults. Journal of Neurophysiology 90, 755–762. Pai, Y.-C., Yang, F., Wening, J.D., Pavol, M.J., in press. Mechanisms of limb collapse following a slip among young and older adults. Journal of Biomechanics, in press. 23 August 2005 [Epub ahead of print]. Pavol, M.J., Owings, T.M., Foley, K.T., Grabiner, M.D., 2001. Mechanisms leading to a fall from an induced trip in healthy older adults. Journal of Gerontology: Medical Sciences 56A, M428–M437. Pavol, M.J., Owings, T.M., Grabiner, M.D., 2002a. Body segment inertial parameter estimation for the general population of older adults. Journal of Biomechanics 35, 707–712.

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Pavol, M.J., Runtz, E.F., Edwards, B.J., Pai, Y.-C., 2002b. Age influences the outcome of a slipping perturbation during initial but not repeated exposures. Journal of Gerontology: Medical Sciences 57A, M496–M503. Pavol, M.J., Runtz, E.F., Pai, Y.-C., 2004a. Diminished stepping responses lead to a fall following a novel slip induced during a sitto-stand. Gait and Posture 20, 154–162. Pavol, M.J., Runtz, E.F., Pai, Y.-C., 2004b. Young and older adults exhibit proactive and reactive adaptations to repeated slip exposure. Journal of Gerontology: Medical Sciences 59A, 494–502. Pijnappels, M., Bobbert, M.F., van Dieen, J.H., 2004. Contribution of the support limb in control of angular momentum after tripping. Journal of Biomechanics 37, 1811–1818. Pijnappels, M., Bobbert, M.F., van Dieen, J.H., 2005. Push-off reactions in recovery after tripping discriminate young subjects, older non-fallers, and older fallers. Gait and Posture 21, 388–394. Podsiadlo, D., Richardson, S., 1991. The timed ‘‘Up & Go’’: a test of basic functional mobility for frail persons. Journal of the American Geriatrics Society 39, 142–148. Robinovitch, S.N., Brumer, R., Maurer, J., 2004. Effect of the ‘‘squat protective response’’ on impact velocity during backward falls. Journal of Biomechanics 37, 1329–1337. Sandler, R., Robinovitch, S., 2001. An analysis of the effect of lower extremity strength on impact severity during a backward fall. Journal of Biomechanical Engineering 123, 590–598. Schot, P.K., Knutzen, K.M., Poole, S.M., Mrotek, L.A., 2003. Sit-tostand performance of older adults following strength training. Research Quarterly for Exercise and Sport 74, 1–8. Stel, V.S., Smit, J.H., Pluijm, S.M., Lips, P., 2004. Consequences of falling in older men and women and risk factors for health service use and functional decline. Age and Ageing 33, 58–65. Stelmach, G.E., Teasdale, N., Di Fabio, R.P., Phillips, J., 1989. Age related decline in postural control mechanisms. International Journal of Aging and Human Development 29, 205–223. Tinetti, M.E., Speechley, M., Ginter, S.F., 1988. Risk factors for falls among elderly persons living in the community. New England Journal of Medicine 319, 1701–1707.