- Email: [email protected]
The effect of lower limb muscle fatigue on obstacle negotiation during walking in older adults
Gait & Posture 37 (2013) 506–510
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
The effect of lower limb muscle fatigue on obstacle negotiation during walking in older adults Anna L. Hatton a,*, Jasmine C. Menant b, Stephen R. Lord b, Joanne C.M. Lo b, Daina L. Sturnieks b a b
School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, QLD 4072, Australia Falls and Balance Research Group, Neuroscience Research Australia, University of New South Wales, Randwick, NSW 2031, Australia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 February 2012 Received in revised form 31 July 2012 Accepted 4 September 2012
Tripping over obstacles is a common cause of falls in older adults, and muscle fatigue, which can alter walking patterns, may add to this risk. To date, no study has examined the effect of lower limb muscle fatigue on obstacle negotiation in older adults. 30 older adults (13 women, aged 78.3 [6.2] years) negotiated a 12 m obstacle course, while completing a visual secondary task, under two randomized conditions: rested or fatigued. For the fatigue condition, participants performed a repeated sit-to-stand movement, as fast as possible, until they could no longer continue. Participants then immediately began walking trials. Kinematic and kinetic data were collected on approach to, during, and after crossing a height-adjustable target obstacle (10% and 20% of leg length). Repeated measures ANOVA showed a statistically significant increase in lead limb vertical loading rate after stepping over the 10% obstacle when fatigued, relative to rested (P = 0.046). No other significant between-condition differences (>0.05) were observed for the other kinematic variables when negotiating the 10% obstacle. Furthermore, no significant between-condition differences (P > 0.05) were observed for any kinetic or kinematic variables when negotiating the 20% obstacle. This study describes a feasible method for investigating the consequences of lower limb muscle fatigue on obstacle crossing. The current finding of increased vertical loading rate when fatigued supports the need for further investigation into the effect of muscle fatigue on gait under different environmental conditions, fatiguing a range of muscles, analyzing a more comprehensive array of kinetic and kinematic measures, and in healthy and clinical populations. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Muscle fatigue Obstacle negotiation Gait Aged
1. Introduction Tripping over obstacles commonly causes older people to fall when walking in challenging environments, accounting for 35– 53% of all falls in community-dwelling older people [1]. Previous work has explored obstacle avoidance during walking in a range of older population groups including healthy older people [2–7], older fallers [7–9], and people with Parkinson’s disease [10], stroke [11], and knee osteoarthritis [12]. Successful obstacle avoidance may be compromised by age-related declines in physical function or alterations in motor control strategies [13,14]. Muscular fatigue can lead to a loss of muscle strength, which may compromise obstacle clearance. Evidence from a recent systematic review suggests muscle fatigue can impair standing balance, and functional task performance, specifically response to external perturbation and voluntary movements, in older people [15]. However, only two studies have experimentally investigated
* Corresponding author at: School of Health and Rehabilitation Sciences, Therapies Building (84A), The University of Queensland, QLD 4072, Australia. Tel.: +61 7 3896 3069. E-mail address: [email protected] (A.L. Hatton). 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.09.004
the effect of lower limb muscle fatigue on walking in older people [16,17]. Helbostad et al. [17] concluded that after performing a fatiguing repeated sit-to-stand task, older adults took significantly wider steps, showed greater step length variability and alterations in trunk acceleration during level-ground walking, compared to when rested [17]. The direction of change in these gait variables suggests fatigue may reduce dynamic stability, leading to characteristic walking patterns seen in frail older adults [18,19]. In contrast and surprisingly, Granacher et al. [16] reported that fatigue of the knee extensors (following an isokinetic exercise protocol) in older people, significantly increased gait velocity and stride length and reduced stride length variability under dual-task walking conditions. These conflicting studies [16,17] suggest more research is required to understand the effects of lower limb muscle fatigue on walking in older people under single and dual-task conditions. It also remains unknown whether lower limb muscle fatigue affects obstacle avoidance in older people – an important strategy for avoiding tripping in challenging environments. This study investigated the effects of exercise-induced lower limb muscle fatigue on obstacle negotiation in older people. A visual secondary task was used to emulate a situation encountered during daily life, i.e. navigating through a
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challenging and distracting environment such as a shopping mall or busy street. Previous research has shown that a visual secondary task is necessary to induce obstacle contacts in a laboratory situation [5]. We hypothesized that in negotiating an obstacle, lower limb muscle fatigue would result in: (i) reduced foot clearance; (ii) slower crossing velocity; and (iii) altered limb loading post-obstacle clearance. 2. Methods 2.1. Participants Community-dwelling men and women aged over 70 years were recruited from a volunteer database and advertising at community group meetings. Exclusion criteria included self-reported neuromuscular disease, recent injury to the back or legs, unstable psychiatric conditions, inability to walk 12 m unassisted, and cognitive impairment (Mini-Mental State Examination [MMSE] score <24) [20]. All participants gave written informed consent. Ethical approval was granted by the University of New South Wales Human Research Ethics Committee. 2.2. Baseline assessment Participants completed a short questionnaire detailing current health status. Sensorimotor function, risk of falling, and concern about falling were assessed using the Physiological Profile Assessment [21] and Iconographical Falls Efficacy Scale [22]. 2.3. Equipment Kinematic data were collected using two CODA scanner units (Model cx1, Codamotion, Charnwood Dynamics Ltd., Rothley, UK) at a sampling rate of 200 Hz. Kinetic data was obtained from a Kistler force platform (Model 9286AA, Kistler, Alton, UK) at 1000 Hz. 2.4. Procedures All participants negotiated a 12 m obstacle course, while completing a visual secondary task, under two randomized conditions: rested (control) and fatigued. The 12 m walking path comprised 7 obstacles made from foam and cardboard (smallest [width (distance across the walkway) height length]: 53 0.5 3 cm; largest: 110 18 6 cm), placed at irregular intervals along the walkway (ranging from 0.80 to 2.15 m apart). The sixth obstacle along the walkway was height-adjustable. This ‘target’ obstacle was set to two different height conditions: 10% and 20% of each participant’s leg length (distance from the anterior superior iliac spine to the lateral malleoli of the dominant leg). These heights were chosen based on previous protocols [4,12,23] and represented obstacle dimensions commonly encountered in daily life such as paving curbs [23]. The target obstacle was located directly before a force platform so participants’ lead limb would land on the force platform after crossing the obstacle. The order of target obstacle height presentation was randomized within-session. Participants wore low-cut ankle socks and Oxford-style lace-up shoes of the appropriate size with a suede upper and nitrile rubber sole during testing. Active markers were attached bilaterally onto the toe box, fifth metatarsal head, most posterior position on the left heel (facing laterally) and right heel (facing medially), left lateral malleolus, right medial malleolus, and top surface of the target obstacle. Prior to testing, the investigator ensured marker wire connections did not impede walking ability. 2.4.1. Walking task At the starting line, participants received standardized instructions to walk at their preferred speed, step over the obstacles, and were encouraged not to stop during trials. Following a practice trial, participants navigated the walkway six times for each obstacle height for a total 12 consecutive trials per session. Participants were instructed to commence each gait trial by stepping with the same foot, to ensure they crossed the target obstacle with the same lead limb. Fig. 1 illustrates the kinematic measures collected. Vertical loading rate of the lead limb, after stepping over the target obstacle, was calculated from the vertical force recorded over the first 100 ms of foot contact with the force platform and normalized to subjects’ body mass (expressed in N kg 1 s 1) [24]. A threshold of 10 N was used to identify onset of foot contact [25]. Vertical loading rate was normalized to walking velocity (expressed in N kg 1 m 1) [24] to ensure any significant differences in kinetic variables between rested and fatigue conditions were not caused by variations in walking velocity. 2.4.2. Visual secondary task Whilst negotiating the obstacle course, participants were required to regularly look up and read aloud a sequence of 10 monosyllabic letters (C, D, E, F, L, N, O P, T and Z) from a computer screen positioned at eye level at the end of the walkway (12.5 m from the start). Letters were displayed in Arial font (height: 261 mm, width:
Fig. 1. Kinematic measures collected on approach to, during, and after crossing the target obstacle set to 10% and 20% of leg length. (a) Trail limb approach distance (trail limb toe-obstacle horizontal distance on approach) (cm). (b) Trail limb toe clearance (trail limb toe-obstacle vertical distance at toe crossing) (cm). (c) Lead limb heel clearance (lead limb heel-obstacle vertical distance at heel crossing) (cm). (d) Lead limb landing distance (lead limb heel-obstacle horizontal distance after stepping over obstacle) (cm). (e) Obstacle crossing stride length (horizontal distance between trail limb heel contact on approach to obstacle and trail limb heel contact after stepping over obstacle) (cm). (f) Obstacle crossing velocity (stride length over obstacle/obstacle crossing time) (m s 1). 224 mm and limb thickness: 34 mm), and presented for 1.5 s, followed by a blank screen presented for 2 s break. An auditory cue signaled the presentation of each letter [5]. 2.4.3. Fatigue protocol The term fatigue was defined as ‘the observation of a decrement in performance following exercise’ [15]. Participants sat on a 66 cm hardback chair. A Velcro strap, to which a digital strain gauge was connected, was attached to the participant’s leg, 10 cm above the lateral malleolus of the dominant lower limb. Participants extended their knee as hard as they could against the resistance of the strap. This procedure was repeated three times to generate a measure of pre-fatigue quadriceps muscle strength. Participants then transferred to a 46 cm hardback chair and were instructed to cross their arms and repeatedly stand up and sit down as fast as possible (while receiving verbal encouragement), until they could no longer continue [17]. The number of sit-to-stand repetitions was counted and timed. Immediately after the participant indicated they could no longer continue, quadriceps muscle strength was re-assessed. Participants then immediately began walking trials. Rested and fatigued conditions were randomly presented and performed on two separate occasions, approximately one week apart, providing sufficient recovery time for those who completed the fatigued trials first. 2.5. Statistical analysis Data were analyzed with SPSS (Chicago, IL, USA) version 18.0.0. For each variable, a repeated measures analysis of variance (ANOVA) was conducted to determine the within-subject effects of lower limb muscle fatigue (for the 10% and 20% obstacles) on kinematic and kinetic variables. Rested obstacle crossing velocity (for each obstacle height), was included as a covariate. The alpha was set at 0.05 with Bonferroni adjustments for multiple comparisons.
3. Results Of the 43 participants recruited, 3 were excluded prior to data collection, one due to ill health and two were unable to walk 12 m unassisted. Following data collection, 10 participants were excluded from the final analysis, as they showed no decrement in quadriceps muscle strength after performing the fatiguing task. Table 1 shows basic demographic, health, and sensorimotor function measures, for the 30 included participants. In the current study, older people walked at a mean (SD) velocity of 0.95 (0.25) m s 1 and 0.88 (0.24) m s 1, when crossing the low-level and high-level target obstacles during the rested condition, respectively. These data suggest the functioning level of healthy older participants in the current study concurs with previous research strategies investigating obstacle crossing in healthy older people (mean crossing speed 0.82–2.16 m s 1) [6]. 3.1. Fatiguing task The mean (SD) number of sit-to-stand repetitions performed was 62.5 (39.6), range 23–202, in a duration of 154.1 (108.3) s.
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Table 1 Basic demographic, health, and sensorimotor function measures (n = 30). Sample characteristics
Mean SD/n (%)
Basic demographics Women Age (years) Weight (kg) Height (m) Dominant leg length (cm) Body mass index (kg/m2) MMSEa score
13 (43.33) 78.27 6.16 (range 70–90) 74.35 15.5 (range 49.40–116.40) 1.65 0.08 (range 1.44–1.80) 89.33 4.60 (range 76.0–99.0) 27.24 4.77 (range 19.72–38.89) 29.40 1.10 (range 25–30)
kinematic variables when negotiating the 10% obstacle. Furthermore, no significant between-condition differences (P > 0.05) were observed for any kinetic or kinematic variables when negotiating the 20% obstacle. 4. Discussion
Self-reported major medical conditions Cardiovascular 25 (83.33) Respiratory 1 (3.33) Musculoskeletal 23 (76.67) Sensory 14 (46.67) 18 (60.00) Other Falls Older people reporting a fall in the previous 12 months ICON-FESb score Sensorimotor function Edge-contrast sensitivity (dB)c Hand reaction time (ms) Proprioception at the leg (error in) Quadriceps strength (kg) Postural sway while standing on foam with eyes open (mm2)c Falls risk score
4 (13.33) 45.60 16.29 (range 32–98) 21.40 1.38 (range 19.00–24.00) 218 28 (range 165.00–273.10) 1.45 0.98 (range 0.00–3.20) 29.55 11.76 (range 9.54–58.12) 786.77 782.66 (range 50.00–3456.00) 0.13 0.81 (range
1.94 to 2.09)
a
Mini-Mental State Examination [20]; higher scores indicate better performance (possible range 0–30). b Iconographical Falls Efficacy Scale score [22]; higher scores indicate greater concern about falling (possible range 30–120). c Higher score in the test of edge-contrast sensitivity indicates better performance; lower score in the tests of postural sway indicates better performance.
Mean (SD) quadriceps muscle strength decreased by 9.5%, from 32.4 (11.7) kg when rested to 29.7 (10.9) kg post-fatiguing task (P < 0.001). 3.2. Walking task Based on participants’ dominant leg length, the height of the 10% and 20% target obstacles ranged from 7.6 to 9.9 cm and 15.2 to 19.8 cm, respectively. Table 2 shows the results for the kinetic and kinematic data collected for lead and trail limbs during walking trials. Vertical loading rate of the lead limb, after stepping over the 10% target obstacle, was significantly greater when fatigued, relative to rested (P = 0.046). No other significant betweencondition differences (>0.05) were observed for the other
This study examined the effect of exercise-induced lower limb muscle fatigue on obstacle negotiation during walking in healthy older adults. Normalized vertical loading rate of the lead limb, after stepping over a low-level obstacle, was significantly greater when fatigued, compared to rested. An individual’s rate of loading during walking can be influenced by lower limb positioning, velocity, acceleration and ground reaction forces, factors which may be affected by muscle fatigue. Previous studies have shown that exercise-induced muscle fatigue can impair joint positioning and lower limb neuromuscular control in healthy young [26] and older adults [27], and there is evidence that muscle fatigue may impair muscle spindle function, and the accuracy of proprioceptive information [28]. It is possible that knee extensor muscle fatigue may impair proprioception, and resultant alterations in lead limb joint angles upon landing after obstacle crossing may contribute to increases in vertical loading rate. This requires further investigation. Muscle fatigue may have impaired the control of volitional lower limb movement when stepping over the low-level obstacle. This could be attributed to a loss of confidence in predicting leg position and muscle control, and as such, participants may have exaggerated activity in the lead limb hip, knee, and ankle extensors, in order to ensure balance support after stepping, thereafter increasing the vertical loading rate. The greater vertical loading rate observed when fatigued, suggests that participants used the ground to arrest foot motion, rather than muscular activity to slow down progression of the lead limb in a controlled manner. It is also possible that the trailing limb extensor muscles may have been fatigued and did not adequately support the body prior to contralateral (lead limb) foot contact, resulting in higher lead limb vertical loading rate. A number of trends were also observed when negotiating the low-level obstacle. When fatigued, trail limb approach distance (to the obstacle) increased (P = 0.067), whilst lead limb landing distance (P = 0.089) and obstacle crossing stride length (P = 0.052) were shorter relative to rested. It appears that when fatigued, participants encountered the low-level obstacle slightly later, and cleared the obstacle in a shorter step. These findings suggest further investigation is needed to examine whether greater levels of muscle fatigue may lead to similar, more prominent, clinically important changes in foot placement before and after negotiating an obstacle, thereafter increasing
Table 2 Kinetic and kinematic variables for the lead and trail limbs on approach to, during, and after crossing the target obstacle set to 10% and 20% of leg length when rested and fatigued. 10% target obstacle height
Variable
Primary outcome measures Trail limb approach distance (cm) Lead limb heel clearance (cm) Trail limb toe clearance (cm) Obstacle crossing stride length (cm) Obstacle crossing velocity (m s 1) Lead limb landing distance (cm) Vertical loading rate of lead limb (N kg * a
1
m
1
)
20% target obstacle height
N=
Rested mean (SD)
Fatigued mean (SD)
P-value
N=
Rested mean (SD)
Fatigued mean (SD)
P-value
29a 30 25a 30 30 30 29a
27.16 12.98 16.20 133.90 0.95 20.23 77.84
27.74 12.35 16.35 131.85 0.93 18.60 82.57
0.067 0.383 0.415 0.052 0.576 0.089 0.046*
30 30 27a 30 30 30 29a
25.43 12.12 14.75 132.60 0.88 19.92 83.54
25.20 12.34 16.46 132.33 0.86 19.83 83.63
0.834 0.463 0.896 0.088 0.485 0.419 0.420
(8.74) (4.36) (6.97) (21.75) (0.25) (9.10) (16.10)
(7.87) (5.05 (4.81) (21.44) (0.23) (7.87) (18.55)
P < 0.05. Missing data resulting from markers on the shoes being out of view or corrupt force platform output.
(5.36) (4.04) (5.89) (20.73) (0.24) (8.40) (13.17)
(4.87) (4.34) (5.93) (21.98) (0.23) (8.39) (16.39)
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the likelihood of contacting an obstacle and risk of experiencing a trip or fall. Previous research suggests that taking shorter steps, is one characteristic change in gait observed in older people who adopt a conservative walking pattern in order to maintain balance [29]. It is possible that lower limb muscle fatigue may impair dynamic balance control in older people during obstructed walking. However, the significant alteration observed in vertical loading rate, and trends noticed in foot distance from the obstacle (resulting from lower limb muscle fatigue), could be detrimental to successful obstacle negotiation, increasing participants’ risk of experiencing a trip and fall. A more comprehensive analysis of lower limb kinetic and kinematic measures is needed. Helbostad et al. [17] reported that lower limb muscle fatigue can lead to significant changes in gait variables during unobstructed walking, specifically step width, stride length variability, trunk acceleration and trunk acceleration variability. In the current study we did not calculate these gait parameters, as we were only interested in variables associated with obstacle crossing. Granacher et al. [16] concluded that when fatigued, older adults took longer strides and walked at a faster velocity under dual-task conditions, compared to control. These changes in gait variables suggest participants were able to execute compensatory strategies to overcome fatigue effects and maintain function. Sample characteristics including age, height, weight, and cognitive ability were similar between the current study and previous work by Granacher et al. [16] and Helbostad et al. [17], however our findings are more in line with those of Helbostad et al. [17] suggesting that lower limb muscle fatigue impairs gait performance in older people. In the current study, the significant increase in vertical loading rate and trends for alterations in horizontal foot position and stride length were only observed when negotiating the low-level obstacle (10% leg length) This may be related to different attentional demands. When negotiating the high-level obstacle, participants may have been more attentive to ensure successful negotiation of this greater gait challenge. Therefore, changes observed in kinetic and kinematic variables during low-level obstacle crossing may be attributed to relative inattention, combined with fatigue. It is possible that the visual secondary task may have provided sufficient distraction, and indeed been prioritized, when negotiating the low-level obstacle, so that participants were less attentive to their foot placement or obstacle crossing technique during the lesser gait challenge. It was not within the aims of this study to explore prioritization of tasks, however this is an important area for future research. The fatigue protocol used in this study has previously been shown to fatigue lower limb muscles in older people. However, the ability to continue performing the fatiguing task may have been limited by participant’s aerobic capacity rather than muscular fatigue. Indeed, 10 participants were excluded from the analysis as they showed no decrement in knee extensor muscle strength postfatiguing task. Although participants received verbal encouragement during the fatiguing task, lack of motivation may also have been a limiting factor. 5. Conclusion The current study provides preliminary evidence that lower limb fatigue may impair movement control and foot positioning in older people before, and after negotiating low-level obstacles. This study describes a feasible method for investigating the consequences of exercise-induced lower limb muscle fatigue on obstacle crossing in older people. The current finding of increased
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vertical loading rate when fatigued compared to rested, supports the need for further investigation into the effect of muscle fatigue on gait under different environmental conditions, fatiguing a range of muscles, analyzing a more comprehensive array of kinetic and kinematic measures, and in healthy and clinical populations. Acknowledgements This work was supported by an Endeavour Research Fellowship (Australia Awards) and Baroness Robson Travel Scholarship (Chartered Society of Physiotherapy), awarded to ALH. The study sponsors had no involvement: in the study design; collection, analysis and interpretation of data; in the writing or submission of this manuscript. Conflict of interest statement The authors have no conflicts of interest to declare. References [1] Lord S, Ward J, Williams P, Anstey K. An epidemiological study of falls in older community-dwelling women: the Randwick falls and fracture study. Australian and New Zealand Journal of Public Health 1993;17(3):240–5. [2] Chen H, Schultz A, Asgton-Miller J, Giordani B, Alexander N, Guire K. Stepping over obstacles: dividing attention impairs performance of old more than young adults. Journals of Gerontology Series A Biological Sciences and Medical Sciences 1996;51A(3):116–22. [3] Hahn M, Lee H, Chou L. Increased muscular challenge in older adults during obstructed gait. Gait and Posture 2005;22:356–61. [4] Lu T, Chen H, Chen S. Comparisons of the lower limb kinematics between young and older adults when crossing obstacles of different heights. Gait and Posture 2006;23:471–9. [5] Menant J, St George R, Fitzpatrick R, Lord S. Impaired depth perception and restricted pitch head movement increase obstacle contacts when dual-tasking in older people. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2010;65A(7):751–7. [6] Schrodt L, Mercer V, Giuliani C, Hartman M. Characteristics of stepping over an obstacle in community dwelling older adults under dual-task conditions. Gait and Posture 2004;19:279–87. [7] Uemura K, Yamada M, Nagai K, Ichihashi N. Older adults at high risk of falling need more time for anticipatory postural adjustment in the precrossing phase of obstacle negotiation. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2011;66A(8):904–9. [8] Di Fabio R, Kurszewski W, Jorgenson E, Kunz R. Footlift asymmetry during obstacle avoidance in high-risk elderly. Journal of the American Geriatrics Society 2004;52:2088–93. [9] Newstead A, Walden J, Gitter A. Gait variables differentiating fallers from nonfallers. Journal of Geriatric Physical Therapy 2007;30(3):93–101. [10] Vitorio R, Pieruccini-Faria F, Stella F, Gobbi S, Gobbi L. Effects of obstacle height on obstacle crossing in mild Parksinson’s disease. Gait and Posture 2010;31:143–6. [11] Said C, Goldie P, Culham E, Sparrow W, Patla A, Morris M. Control of lead and trail limbs during obstacle crossing following stroke. Physical Therapy 2005;85(5):413–27. [12] Lu T, Chen H, Wang T. Obstacle crossing in older adults with medial compartment knee osteoarthritis. Gait and Posture 2007;26:553–9. [13] Galna B, Peters A, Murphy A, Morris M. Obstacle crossing deficits in older adults: a systematic review. Gait and Posture 2009;30:270–5. [14] Kovacs C. Age-related changes in gait and obstacle avoidance capabilities in older adults: a review. Journal of Applied Gerontology 2005;24(1):21–34. [15] Helbostad J, Sturnieks D, Menant J, Delbaere K, Lord S, Pijnappels M. Consequences of lower extremity and trunk muscle fatigue on balance and functional tasks in older people: a systematic literature review. BMC Geriatrics 2010;10(56). [16] Granacher U, Wolf I, Wehrle A, Brindenbaugh S, Kressig R. Effects of muscle fatigue on gait characteristics under single and dual-task conditions in young and older adults. Journal of NeuroEngineering and Rehabilitation 2010;7(56). [17] Helbostad J, Leirfall S, Moe-Nilssen R, Sletvold O. Physical fatigue affects gait characteristics in older persons. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2007;62A(9):1010–5. [18] Callisaya M, Blizzard L, Schmidt M, Martin K, McGinley J, Sanders L, et al. Gait, gait variability and the risk of multiple incident falls in older people: a population-based study. Age and Ageing 2011;40(4):481–7. [19] Menz H, Lord S, Fitzpatrick R. Acceleration patterns of the head and pelvis when walking are associated with risk of falling in community-dwelling older people. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2003;58(5):M446–52.
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[20] Folstein M, Folstein S, McHugh P. ‘‘Mini-mental state’’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975;12(3):189–98. [21] Lord S, Menz H, Tiedemann A. A physiological profile approach to falls risk assessment and prevention. Physical Therapy 2003;83.:237–52. [22] Delbaere K, Smith S, Lord S. Development and initial validation of the iconographical falls efficacy scale. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2011;66A(6):674–80. [23] Decker L, Houser J, Noble J, Karst G, Stergiou N. The effects of shoe traction and obstacle height on lower extremity coordination dynamics during walking. Applied Ergonomics 2009;40:895–903. [24] Menant J, Perry S, Steele J, Munro B, Lord S. Effects of shoe characteristics on dynamic stability when walking on even and uneven surfaces in young and older people. Archives of Physical Medicine and Rehabilitation 2008;89(10):1970–6.
[25] McCaw S, Heil M, Hamill J. The effect of comments about shoe construction on impact forces during walking. Medicine and Science in Sports and Exercise 2000;32(7):1258–64. [26] Lattanzio P, Petrella R, Sproule J, Fowler P. Effects of fatigue on knee proprioception. Clinical Journal of Sport Medicine 1997;7(1):22–7. [27] Ribeiro F, Mota J, Oliveira J. Effect of exercise-induced fatigue on position sense of the knee in the elderly. European Journal of Applied Physiology 2007;99:379–85. [28] Hiemstra L, Lo I, Fowler P. Effect of fatigue on knee proprioception: implications for dynamic stabilization. Journal of Orthopaedic and Sports Physical Therapy 2001;31(10):598–605. [29] Menz H, Lord S, Fitzpatrick R. Age-related differences in walking stability. Age and Ageing 2003;32(2):137–42.
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
The effect of lower limb muscle fatigue on obstacle negotiation during walking in older adults Anna L. Hatton a,*, Jasmine C. Menant b, Stephen R. Lord b, Joanne C.M. Lo b, Daina L. Sturnieks b a b
School of Health and Rehabilitation Sciences, The University of Queensland, Brisbane, QLD 4072, Australia Falls and Balance Research Group, Neuroscience Research Australia, University of New South Wales, Randwick, NSW 2031, Australia
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 February 2012 Received in revised form 31 July 2012 Accepted 4 September 2012
Tripping over obstacles is a common cause of falls in older adults, and muscle fatigue, which can alter walking patterns, may add to this risk. To date, no study has examined the effect of lower limb muscle fatigue on obstacle negotiation in older adults. 30 older adults (13 women, aged 78.3 [6.2] years) negotiated a 12 m obstacle course, while completing a visual secondary task, under two randomized conditions: rested or fatigued. For the fatigue condition, participants performed a repeated sit-to-stand movement, as fast as possible, until they could no longer continue. Participants then immediately began walking trials. Kinematic and kinetic data were collected on approach to, during, and after crossing a height-adjustable target obstacle (10% and 20% of leg length). Repeated measures ANOVA showed a statistically significant increase in lead limb vertical loading rate after stepping over the 10% obstacle when fatigued, relative to rested (P = 0.046). No other significant between-condition differences (>0.05) were observed for the other kinematic variables when negotiating the 10% obstacle. Furthermore, no significant between-condition differences (P > 0.05) were observed for any kinetic or kinematic variables when negotiating the 20% obstacle. This study describes a feasible method for investigating the consequences of lower limb muscle fatigue on obstacle crossing. The current finding of increased vertical loading rate when fatigued supports the need for further investigation into the effect of muscle fatigue on gait under different environmental conditions, fatiguing a range of muscles, analyzing a more comprehensive array of kinetic and kinematic measures, and in healthy and clinical populations. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Muscle fatigue Obstacle negotiation Gait Aged
1. Introduction Tripping over obstacles commonly causes older people to fall when walking in challenging environments, accounting for 35– 53% of all falls in community-dwelling older people [1]. Previous work has explored obstacle avoidance during walking in a range of older population groups including healthy older people [2–7], older fallers [7–9], and people with Parkinson’s disease [10], stroke [11], and knee osteoarthritis [12]. Successful obstacle avoidance may be compromised by age-related declines in physical function or alterations in motor control strategies [13,14]. Muscular fatigue can lead to a loss of muscle strength, which may compromise obstacle clearance. Evidence from a recent systematic review suggests muscle fatigue can impair standing balance, and functional task performance, specifically response to external perturbation and voluntary movements, in older people [15]. However, only two studies have experimentally investigated
* Corresponding author at: School of Health and Rehabilitation Sciences, Therapies Building (84A), The University of Queensland, QLD 4072, Australia. Tel.: +61 7 3896 3069. E-mail address: [email protected] (A.L. Hatton). 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.09.004
the effect of lower limb muscle fatigue on walking in older people [16,17]. Helbostad et al. [17] concluded that after performing a fatiguing repeated sit-to-stand task, older adults took significantly wider steps, showed greater step length variability and alterations in trunk acceleration during level-ground walking, compared to when rested [17]. The direction of change in these gait variables suggests fatigue may reduce dynamic stability, leading to characteristic walking patterns seen in frail older adults [18,19]. In contrast and surprisingly, Granacher et al. [16] reported that fatigue of the knee extensors (following an isokinetic exercise protocol) in older people, significantly increased gait velocity and stride length and reduced stride length variability under dual-task walking conditions. These conflicting studies [16,17] suggest more research is required to understand the effects of lower limb muscle fatigue on walking in older people under single and dual-task conditions. It also remains unknown whether lower limb muscle fatigue affects obstacle avoidance in older people – an important strategy for avoiding tripping in challenging environments. This study investigated the effects of exercise-induced lower limb muscle fatigue on obstacle negotiation in older people. A visual secondary task was used to emulate a situation encountered during daily life, i.e. navigating through a
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challenging and distracting environment such as a shopping mall or busy street. Previous research has shown that a visual secondary task is necessary to induce obstacle contacts in a laboratory situation [5]. We hypothesized that in negotiating an obstacle, lower limb muscle fatigue would result in: (i) reduced foot clearance; (ii) slower crossing velocity; and (iii) altered limb loading post-obstacle clearance. 2. Methods 2.1. Participants Community-dwelling men and women aged over 70 years were recruited from a volunteer database and advertising at community group meetings. Exclusion criteria included self-reported neuromuscular disease, recent injury to the back or legs, unstable psychiatric conditions, inability to walk 12 m unassisted, and cognitive impairment (Mini-Mental State Examination [MMSE] score <24) [20]. All participants gave written informed consent. Ethical approval was granted by the University of New South Wales Human Research Ethics Committee. 2.2. Baseline assessment Participants completed a short questionnaire detailing current health status. Sensorimotor function, risk of falling, and concern about falling were assessed using the Physiological Profile Assessment [21] and Iconographical Falls Efficacy Scale [22]. 2.3. Equipment Kinematic data were collected using two CODA scanner units (Model cx1, Codamotion, Charnwood Dynamics Ltd., Rothley, UK) at a sampling rate of 200 Hz. Kinetic data was obtained from a Kistler force platform (Model 9286AA, Kistler, Alton, UK) at 1000 Hz. 2.4. Procedures All participants negotiated a 12 m obstacle course, while completing a visual secondary task, under two randomized conditions: rested (control) and fatigued. The 12 m walking path comprised 7 obstacles made from foam and cardboard (smallest [width (distance across the walkway) height length]: 53 0.5 3 cm; largest: 110 18 6 cm), placed at irregular intervals along the walkway (ranging from 0.80 to 2.15 m apart). The sixth obstacle along the walkway was height-adjustable. This ‘target’ obstacle was set to two different height conditions: 10% and 20% of each participant’s leg length (distance from the anterior superior iliac spine to the lateral malleoli of the dominant leg). These heights were chosen based on previous protocols [4,12,23] and represented obstacle dimensions commonly encountered in daily life such as paving curbs [23]. The target obstacle was located directly before a force platform so participants’ lead limb would land on the force platform after crossing the obstacle. The order of target obstacle height presentation was randomized within-session. Participants wore low-cut ankle socks and Oxford-style lace-up shoes of the appropriate size with a suede upper and nitrile rubber sole during testing. Active markers were attached bilaterally onto the toe box, fifth metatarsal head, most posterior position on the left heel (facing laterally) and right heel (facing medially), left lateral malleolus, right medial malleolus, and top surface of the target obstacle. Prior to testing, the investigator ensured marker wire connections did not impede walking ability. 2.4.1. Walking task At the starting line, participants received standardized instructions to walk at their preferred speed, step over the obstacles, and were encouraged not to stop during trials. Following a practice trial, participants navigated the walkway six times for each obstacle height for a total 12 consecutive trials per session. Participants were instructed to commence each gait trial by stepping with the same foot, to ensure they crossed the target obstacle with the same lead limb. Fig. 1 illustrates the kinematic measures collected. Vertical loading rate of the lead limb, after stepping over the target obstacle, was calculated from the vertical force recorded over the first 100 ms of foot contact with the force platform and normalized to subjects’ body mass (expressed in N kg 1 s 1) [24]. A threshold of 10 N was used to identify onset of foot contact [25]. Vertical loading rate was normalized to walking velocity (expressed in N kg 1 m 1) [24] to ensure any significant differences in kinetic variables between rested and fatigue conditions were not caused by variations in walking velocity. 2.4.2. Visual secondary task Whilst negotiating the obstacle course, participants were required to regularly look up and read aloud a sequence of 10 monosyllabic letters (C, D, E, F, L, N, O P, T and Z) from a computer screen positioned at eye level at the end of the walkway (12.5 m from the start). Letters were displayed in Arial font (height: 261 mm, width:
Fig. 1. Kinematic measures collected on approach to, during, and after crossing the target obstacle set to 10% and 20% of leg length. (a) Trail limb approach distance (trail limb toe-obstacle horizontal distance on approach) (cm). (b) Trail limb toe clearance (trail limb toe-obstacle vertical distance at toe crossing) (cm). (c) Lead limb heel clearance (lead limb heel-obstacle vertical distance at heel crossing) (cm). (d) Lead limb landing distance (lead limb heel-obstacle horizontal distance after stepping over obstacle) (cm). (e) Obstacle crossing stride length (horizontal distance between trail limb heel contact on approach to obstacle and trail limb heel contact after stepping over obstacle) (cm). (f) Obstacle crossing velocity (stride length over obstacle/obstacle crossing time) (m s 1). 224 mm and limb thickness: 34 mm), and presented for 1.5 s, followed by a blank screen presented for 2 s break. An auditory cue signaled the presentation of each letter [5]. 2.4.3. Fatigue protocol The term fatigue was defined as ‘the observation of a decrement in performance following exercise’ [15]. Participants sat on a 66 cm hardback chair. A Velcro strap, to which a digital strain gauge was connected, was attached to the participant’s leg, 10 cm above the lateral malleolus of the dominant lower limb. Participants extended their knee as hard as they could against the resistance of the strap. This procedure was repeated three times to generate a measure of pre-fatigue quadriceps muscle strength. Participants then transferred to a 46 cm hardback chair and were instructed to cross their arms and repeatedly stand up and sit down as fast as possible (while receiving verbal encouragement), until they could no longer continue [17]. The number of sit-to-stand repetitions was counted and timed. Immediately after the participant indicated they could no longer continue, quadriceps muscle strength was re-assessed. Participants then immediately began walking trials. Rested and fatigued conditions were randomly presented and performed on two separate occasions, approximately one week apart, providing sufficient recovery time for those who completed the fatigued trials first. 2.5. Statistical analysis Data were analyzed with SPSS (Chicago, IL, USA) version 18.0.0. For each variable, a repeated measures analysis of variance (ANOVA) was conducted to determine the within-subject effects of lower limb muscle fatigue (for the 10% and 20% obstacles) on kinematic and kinetic variables. Rested obstacle crossing velocity (for each obstacle height), was included as a covariate. The alpha was set at 0.05 with Bonferroni adjustments for multiple comparisons.
3. Results Of the 43 participants recruited, 3 were excluded prior to data collection, one due to ill health and two were unable to walk 12 m unassisted. Following data collection, 10 participants were excluded from the final analysis, as they showed no decrement in quadriceps muscle strength after performing the fatiguing task. Table 1 shows basic demographic, health, and sensorimotor function measures, for the 30 included participants. In the current study, older people walked at a mean (SD) velocity of 0.95 (0.25) m s 1 and 0.88 (0.24) m s 1, when crossing the low-level and high-level target obstacles during the rested condition, respectively. These data suggest the functioning level of healthy older participants in the current study concurs with previous research strategies investigating obstacle crossing in healthy older people (mean crossing speed 0.82–2.16 m s 1) [6]. 3.1. Fatiguing task The mean (SD) number of sit-to-stand repetitions performed was 62.5 (39.6), range 23–202, in a duration of 154.1 (108.3) s.
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Table 1 Basic demographic, health, and sensorimotor function measures (n = 30). Sample characteristics
Mean SD/n (%)
Basic demographics Women Age (years) Weight (kg) Height (m) Dominant leg length (cm) Body mass index (kg/m2) MMSEa score
13 (43.33) 78.27 6.16 (range 70–90) 74.35 15.5 (range 49.40–116.40) 1.65 0.08 (range 1.44–1.80) 89.33 4.60 (range 76.0–99.0) 27.24 4.77 (range 19.72–38.89) 29.40 1.10 (range 25–30)
kinematic variables when negotiating the 10% obstacle. Furthermore, no significant between-condition differences (P > 0.05) were observed for any kinetic or kinematic variables when negotiating the 20% obstacle. 4. Discussion
Self-reported major medical conditions Cardiovascular 25 (83.33) Respiratory 1 (3.33) Musculoskeletal 23 (76.67) Sensory 14 (46.67) 18 (60.00) Other Falls Older people reporting a fall in the previous 12 months ICON-FESb score Sensorimotor function Edge-contrast sensitivity (dB)c Hand reaction time (ms) Proprioception at the leg (error in) Quadriceps strength (kg) Postural sway while standing on foam with eyes open (mm2)c Falls risk score
4 (13.33) 45.60 16.29 (range 32–98) 21.40 1.38 (range 19.00–24.00) 218 28 (range 165.00–273.10) 1.45 0.98 (range 0.00–3.20) 29.55 11.76 (range 9.54–58.12) 786.77 782.66 (range 50.00–3456.00) 0.13 0.81 (range
1.94 to 2.09)
a
Mini-Mental State Examination [20]; higher scores indicate better performance (possible range 0–30). b Iconographical Falls Efficacy Scale score [22]; higher scores indicate greater concern about falling (possible range 30–120). c Higher score in the test of edge-contrast sensitivity indicates better performance; lower score in the tests of postural sway indicates better performance.
Mean (SD) quadriceps muscle strength decreased by 9.5%, from 32.4 (11.7) kg when rested to 29.7 (10.9) kg post-fatiguing task (P < 0.001). 3.2. Walking task Based on participants’ dominant leg length, the height of the 10% and 20% target obstacles ranged from 7.6 to 9.9 cm and 15.2 to 19.8 cm, respectively. Table 2 shows the results for the kinetic and kinematic data collected for lead and trail limbs during walking trials. Vertical loading rate of the lead limb, after stepping over the 10% target obstacle, was significantly greater when fatigued, relative to rested (P = 0.046). No other significant betweencondition differences (>0.05) were observed for the other
This study examined the effect of exercise-induced lower limb muscle fatigue on obstacle negotiation during walking in healthy older adults. Normalized vertical loading rate of the lead limb, after stepping over a low-level obstacle, was significantly greater when fatigued, compared to rested. An individual’s rate of loading during walking can be influenced by lower limb positioning, velocity, acceleration and ground reaction forces, factors which may be affected by muscle fatigue. Previous studies have shown that exercise-induced muscle fatigue can impair joint positioning and lower limb neuromuscular control in healthy young [26] and older adults [27], and there is evidence that muscle fatigue may impair muscle spindle function, and the accuracy of proprioceptive information [28]. It is possible that knee extensor muscle fatigue may impair proprioception, and resultant alterations in lead limb joint angles upon landing after obstacle crossing may contribute to increases in vertical loading rate. This requires further investigation. Muscle fatigue may have impaired the control of volitional lower limb movement when stepping over the low-level obstacle. This could be attributed to a loss of confidence in predicting leg position and muscle control, and as such, participants may have exaggerated activity in the lead limb hip, knee, and ankle extensors, in order to ensure balance support after stepping, thereafter increasing the vertical loading rate. The greater vertical loading rate observed when fatigued, suggests that participants used the ground to arrest foot motion, rather than muscular activity to slow down progression of the lead limb in a controlled manner. It is also possible that the trailing limb extensor muscles may have been fatigued and did not adequately support the body prior to contralateral (lead limb) foot contact, resulting in higher lead limb vertical loading rate. A number of trends were also observed when negotiating the low-level obstacle. When fatigued, trail limb approach distance (to the obstacle) increased (P = 0.067), whilst lead limb landing distance (P = 0.089) and obstacle crossing stride length (P = 0.052) were shorter relative to rested. It appears that when fatigued, participants encountered the low-level obstacle slightly later, and cleared the obstacle in a shorter step. These findings suggest further investigation is needed to examine whether greater levels of muscle fatigue may lead to similar, more prominent, clinically important changes in foot placement before and after negotiating an obstacle, thereafter increasing
Table 2 Kinetic and kinematic variables for the lead and trail limbs on approach to, during, and after crossing the target obstacle set to 10% and 20% of leg length when rested and fatigued. 10% target obstacle height
Variable
Primary outcome measures Trail limb approach distance (cm) Lead limb heel clearance (cm) Trail limb toe clearance (cm) Obstacle crossing stride length (cm) Obstacle crossing velocity (m s 1) Lead limb landing distance (cm) Vertical loading rate of lead limb (N kg * a
1
m
1
)
20% target obstacle height
N=
Rested mean (SD)
Fatigued mean (SD)
P-value
N=
Rested mean (SD)
Fatigued mean (SD)
P-value
29a 30 25a 30 30 30 29a
27.16 12.98 16.20 133.90 0.95 20.23 77.84
27.74 12.35 16.35 131.85 0.93 18.60 82.57
0.067 0.383 0.415 0.052 0.576 0.089 0.046*
30 30 27a 30 30 30 29a
25.43 12.12 14.75 132.60 0.88 19.92 83.54
25.20 12.34 16.46 132.33 0.86 19.83 83.63
0.834 0.463 0.896 0.088 0.485 0.419 0.420
(8.74) (4.36) (6.97) (21.75) (0.25) (9.10) (16.10)
(7.87) (5.05 (4.81) (21.44) (0.23) (7.87) (18.55)
P < 0.05. Missing data resulting from markers on the shoes being out of view or corrupt force platform output.
(5.36) (4.04) (5.89) (20.73) (0.24) (8.40) (13.17)
(4.87) (4.34) (5.93) (21.98) (0.23) (8.39) (16.39)
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the likelihood of contacting an obstacle and risk of experiencing a trip or fall. Previous research suggests that taking shorter steps, is one characteristic change in gait observed in older people who adopt a conservative walking pattern in order to maintain balance [29]. It is possible that lower limb muscle fatigue may impair dynamic balance control in older people during obstructed walking. However, the significant alteration observed in vertical loading rate, and trends noticed in foot distance from the obstacle (resulting from lower limb muscle fatigue), could be detrimental to successful obstacle negotiation, increasing participants’ risk of experiencing a trip and fall. A more comprehensive analysis of lower limb kinetic and kinematic measures is needed. Helbostad et al. [17] reported that lower limb muscle fatigue can lead to significant changes in gait variables during unobstructed walking, specifically step width, stride length variability, trunk acceleration and trunk acceleration variability. In the current study we did not calculate these gait parameters, as we were only interested in variables associated with obstacle crossing. Granacher et al. [16] concluded that when fatigued, older adults took longer strides and walked at a faster velocity under dual-task conditions, compared to control. These changes in gait variables suggest participants were able to execute compensatory strategies to overcome fatigue effects and maintain function. Sample characteristics including age, height, weight, and cognitive ability were similar between the current study and previous work by Granacher et al. [16] and Helbostad et al. [17], however our findings are more in line with those of Helbostad et al. [17] suggesting that lower limb muscle fatigue impairs gait performance in older people. In the current study, the significant increase in vertical loading rate and trends for alterations in horizontal foot position and stride length were only observed when negotiating the low-level obstacle (10% leg length) This may be related to different attentional demands. When negotiating the high-level obstacle, participants may have been more attentive to ensure successful negotiation of this greater gait challenge. Therefore, changes observed in kinetic and kinematic variables during low-level obstacle crossing may be attributed to relative inattention, combined with fatigue. It is possible that the visual secondary task may have provided sufficient distraction, and indeed been prioritized, when negotiating the low-level obstacle, so that participants were less attentive to their foot placement or obstacle crossing technique during the lesser gait challenge. It was not within the aims of this study to explore prioritization of tasks, however this is an important area for future research. The fatigue protocol used in this study has previously been shown to fatigue lower limb muscles in older people. However, the ability to continue performing the fatiguing task may have been limited by participant’s aerobic capacity rather than muscular fatigue. Indeed, 10 participants were excluded from the analysis as they showed no decrement in knee extensor muscle strength postfatiguing task. Although participants received verbal encouragement during the fatiguing task, lack of motivation may also have been a limiting factor. 5. Conclusion The current study provides preliminary evidence that lower limb fatigue may impair movement control and foot positioning in older people before, and after negotiating low-level obstacles. This study describes a feasible method for investigating the consequences of exercise-induced lower limb muscle fatigue on obstacle crossing in older people. The current finding of increased
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vertical loading rate when fatigued compared to rested, supports the need for further investigation into the effect of muscle fatigue on gait under different environmental conditions, fatiguing a range of muscles, analyzing a more comprehensive array of kinetic and kinematic measures, and in healthy and clinical populations. Acknowledgements This work was supported by an Endeavour Research Fellowship (Australia Awards) and Baroness Robson Travel Scholarship (Chartered Society of Physiotherapy), awarded to ALH. The study sponsors had no involvement: in the study design; collection, analysis and interpretation of data; in the writing or submission of this manuscript. Conflict of interest statement The authors have no conflicts of interest to declare. References [1] Lord S, Ward J, Williams P, Anstey K. An epidemiological study of falls in older community-dwelling women: the Randwick falls and fracture study. Australian and New Zealand Journal of Public Health 1993;17(3):240–5. [2] Chen H, Schultz A, Asgton-Miller J, Giordani B, Alexander N, Guire K. Stepping over obstacles: dividing attention impairs performance of old more than young adults. Journals of Gerontology Series A Biological Sciences and Medical Sciences 1996;51A(3):116–22. [3] Hahn M, Lee H, Chou L. Increased muscular challenge in older adults during obstructed gait. Gait and Posture 2005;22:356–61. [4] Lu T, Chen H, Chen S. Comparisons of the lower limb kinematics between young and older adults when crossing obstacles of different heights. Gait and Posture 2006;23:471–9. [5] Menant J, St George R, Fitzpatrick R, Lord S. Impaired depth perception and restricted pitch head movement increase obstacle contacts when dual-tasking in older people. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2010;65A(7):751–7. [6] Schrodt L, Mercer V, Giuliani C, Hartman M. Characteristics of stepping over an obstacle in community dwelling older adults under dual-task conditions. Gait and Posture 2004;19:279–87. [7] Uemura K, Yamada M, Nagai K, Ichihashi N. Older adults at high risk of falling need more time for anticipatory postural adjustment in the precrossing phase of obstacle negotiation. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2011;66A(8):904–9. [8] Di Fabio R, Kurszewski W, Jorgenson E, Kunz R. Footlift asymmetry during obstacle avoidance in high-risk elderly. Journal of the American Geriatrics Society 2004;52:2088–93. [9] Newstead A, Walden J, Gitter A. Gait variables differentiating fallers from nonfallers. Journal of Geriatric Physical Therapy 2007;30(3):93–101. [10] Vitorio R, Pieruccini-Faria F, Stella F, Gobbi S, Gobbi L. Effects of obstacle height on obstacle crossing in mild Parksinson’s disease. Gait and Posture 2010;31:143–6. [11] Said C, Goldie P, Culham E, Sparrow W, Patla A, Morris M. Control of lead and trail limbs during obstacle crossing following stroke. Physical Therapy 2005;85(5):413–27. [12] Lu T, Chen H, Wang T. Obstacle crossing in older adults with medial compartment knee osteoarthritis. Gait and Posture 2007;26:553–9. [13] Galna B, Peters A, Murphy A, Morris M. Obstacle crossing deficits in older adults: a systematic review. Gait and Posture 2009;30:270–5. [14] Kovacs C. Age-related changes in gait and obstacle avoidance capabilities in older adults: a review. Journal of Applied Gerontology 2005;24(1):21–34. [15] Helbostad J, Sturnieks D, Menant J, Delbaere K, Lord S, Pijnappels M. Consequences of lower extremity and trunk muscle fatigue on balance and functional tasks in older people: a systematic literature review. BMC Geriatrics 2010;10(56). [16] Granacher U, Wolf I, Wehrle A, Brindenbaugh S, Kressig R. Effects of muscle fatigue on gait characteristics under single and dual-task conditions in young and older adults. Journal of NeuroEngineering and Rehabilitation 2010;7(56). [17] Helbostad J, Leirfall S, Moe-Nilssen R, Sletvold O. Physical fatigue affects gait characteristics in older persons. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2007;62A(9):1010–5. [18] Callisaya M, Blizzard L, Schmidt M, Martin K, McGinley J, Sanders L, et al. Gait, gait variability and the risk of multiple incident falls in older people: a population-based study. Age and Ageing 2011;40(4):481–7. [19] Menz H, Lord S, Fitzpatrick R. Acceleration patterns of the head and pelvis when walking are associated with risk of falling in community-dwelling older people. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2003;58(5):M446–52.
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