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Effects of submaximal fatiguing contractions on the components of dynamic stability control after forward falls
Journal of Electromyography and Kinesiology 21 (2011) 270–275
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Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Effects of submaximal fatiguing contractions on the components of dynamic stability control after forward falls Mark Walsh a,⇑, Andreas Peper b,c, Stefanie Bierbaum b,c, Kiros Karamanidis c, Adamantios Arampatzis b a
Department of Kinesiology and Health, Miami University, Oxford, OH 45056, USA Department of Training and Movement Sciences, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 11, 10115 Berlin, Germany c Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Carl-Diem-Weg 6, D-50933 Cologne, Germany b
a r t i c l e
i n f o
Article history: Received 5 February 2010 Received in revised form 7 December 2010 Accepted 10 December 2010
Keywords: Margin of stability Falling Fatigue Muscle strength
a b s t r a c t The present study aimed to investigate the effect of lower extremity muscle fatigue on the dynamic stability control of physically active adults during forward falls. Thirteen participants (body mass: 70.2 kg, height: 175 cm) were instructed to regain balance with a single step after a sudden induced fall from a forward-leaning position before and after the fatigue protocol. The ground reaction forces were collected using four force plates at a sampling rate of 1080 Hz. Kinematic data were recorded with 12 vicon cameras operating at 120 Hz. Neither the reaction time nor the duration until touchdown showed any differences (p > 0.05). The ability of the subjects to prevent falling did not change after the fatigue protocol. In the fatigued condition, the participants demonstrated an increase in knee flexion during the main stance phase and an increased time to decelerate the horizontal CM motion (both p < 0.05). Significant (p < 0.05) decreases were seen post-fatigue in average horizontal and vertical force and maximum knee and ankle joint moments. The fatigue related decrease in muscle strength did not affect the margin of stability, the boundary of the base of support or the position of the extrapolated centre of mass during the forward induced falls, indicating an appropriate adjustment of the motor commands to compensate the deficit in muscle strength. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Falls are an inherent part of life for most everyone. A number of factors may contribute to falls. Many studies have examined static and dynamic balance situations in an attempt to learn more about how the human system controls stability and prevents falls. Although aging is a common focus of balance literature, a loss of muscular strength can also be induced through means other than aging, such as fatigue (Yeung et al., 1999; Moritani et al., 1990). Several studies reported that loss of muscle strength may alter the capacity of the human system to generate rapid force for balance corrections after sudden perturbations (Granacher et al., 2008; Pijnappels et al., 2005; Simoneau and Corbeil, 2005). Karamanidis and Arampatzis (2007) reported that muscle–tendon capacities of the lower limbs contribute about 33% to balance recovery after forward induced falls. However, postural corrections after a sudden perturbation involve sensorimotor adaptational responses which include mechanisms responsible for maintaining the dynamic stability and thus muscle weakness may be partly compensated for by proper planning and execution of the used locomotion strategy. By using fatigued younger subjects to test
⇑ Corresponding author. Tel.: +1 513 529 2708; fax: +1 513 529 5006. E-mail address: [email protected] (M. Walsh). 1050-6411/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2010.12.005
the effects of muscular strength on forward falls we can control for the other changes that occur with aging. Three mechanisms have been presented (Hof, 2007) by which stability may be maintained; by (1) increasing the base of support with relation to the extrapolated centre of mass, (2) counter rotating segments around the CM, and (3) applying an external force other than the ground reaction force (e.g. grasping a handrail or secure object). Examining the human’s capabilities to regain balance after sudden release from a forward inclined body position is a common way to assess dynamic stability (Hsiao and Robinovitch, 1999; Thelen et al., 1997; Wojcik et al., 2001). The margin of stability during locomotion can be quantified by the position of the extrapolated centre of mass (CM) in relation to the base of support (Hof et al., 2005). When the position of the extrapolated CM exceeds the anterior boundary of the base of support, the result is a loss of stability (Hof et al., 2005). Although studies regarding either fatigue or balance are numerous, to date only one study we found has examined the effects of fatigue on dynamic stability control (Mademli et al., 2008). This study found that fatigue had no effect on the components of dynamic stability. However, the fatigue protocol for this study used the knee extension exercise and therefore only fatigued the knee extensor muscles. Preventing a forward fall requires a motion from the front leg that is similar to a lunge and requires not only the knee extensor muscles, but also hip and ankle muscles. The knee extension is a single joint movement requiring
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force production from one muscle group and has little relevance to normal human movement. Additionally, it has been reported that to regain balance during forward falls, extensor muscles from the major lower extremity joints (hip, knee and ankle) are all important (Pijnappels et al., 2005; Madigan and Lloyd, 2005). Therefore the purpose of the present study is to experimentally investigate the effect of fatigue of the lower extremity, induced by submaximal fatiguing contractions, on the dynamic stability control of young adults during forward falls. We hypothesize that dynamic stability will be compromised when the lower extremity is fatigued. This could be seen in a decrease in the ability to regain balance after an induced forward fall.
2. Methods Thirteen participants (7 men and 6 women), age 27.7 ± 4.5 years, body mass: 70.2 ± 13.1 kg, body height: 175 ± 11.1 cm, participated in this study. Before the initiation of this experiment, the procedures were explained to the subjects and informed consent protocol was followed in accordance with the rules of the University Human Subjects Board. Subjects were instructed to regain balance with a single step after a sudden induced fall from a forward-leaning position both before and after a fatiguing protocol targeting the lower extremity. The experiment was performed at the maximal individual lean angle of each participant (maximal forward incline position was where the subjects were able to regain balance with a single step after the sudden release of a support cable which supported them from behind). The force on the cable at maximum lean position was between 25–40% bodyweight. The maximal individual lean angle was determined experimentally before the main experiment. After a short rest (5 min) subjects were tested at their previously measured maximum lean angle. The experimental design of the balance recovery task has been previously described (Karamanidis and Arampatzis, 2007). Following the determination of the subject’s maximum lean angle from which they can be released and still catch themselves, all subjects performed a maximum voluntary isometric squat. Subjects performed the isometric squat with a knee angle of approximately 110 °C. The knee angle was controlled using a goniometer. The isometric squats were performed on a force platform with an adjustable squat bar that was fixed at a height so that the subject’s knee angle was approximately 110 °C. The maximum measured force as measured by the force platform was considered the isometric squat maximum. For the fatigue protocol, subjects were instructed to perform dynamic squats from an extended knee angle of approximately 180 °C to a lower position of approximately 90 °C. The weight used during the fatiguing protocol was 30% of their maximum isometric squat. The dynamic squats were performed with free weights. Once they reached the extended leg position they immediately started moving down again to eliminate the chance of ‘resting’ during the fatigue protocol. Three spotters were present during the fatigue protocol to help the subject with the last repetitions and to help place the bar on the squat rack. The dynamic squat sets were completed until voluntary exhaustion. After 1 min of rest another set of squats was performed and this was repeated until each given subject performed four sets. Directly after the fatigue protocol, the maximum isometric squat of each subject was tested again to measure the extent of the fatigue. Then, immediately after the post maximum isometric squat (30 s) the ability of the subject’s to regain balance with a single step after a sudden induced fall was tested again at their maximum lean angle to see if fatigue affected their dynamic stability control. Following the post induced fall trial, the maximum isometric squat was again tested to document any recovery that may have occurred.
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3. Equipment Kinematic data were tracked using a Vicon Motion Capture System using 12 vicon cameras operating at 120 Hz. Thirty-eight reflective markers (diameter 14 mm) were fixed to landmarks of each subject to aid in motion capture. This included a headband that had four markers on it. The whole body model was used to calculate joint angles, the parameters of dynamic stability and the resultant joint moments through inverse dynamics. We used data provided by Zatsiorsky and Selujanov (1983) to calculate masses and moments of inertia of the body segments. For the trials of each subject, the release, touchdown and minimum knee joint angle were identified. The time of release was defined as the moment the cable holding the subjects in a forward lean was released. Touchdown was defined as the moment the recovery leg contacted the ground after the step. This event was identified using a Kistler force plate (60 90 cm, Kistler, Winterhur, Switzerland, trigger was force exceeding 20 N). Minimum knee angle corresponded with the vertical velocity of the subject reaching a value close to 0 m/s. Using those three points, two recovery phases were identified: (1) phase until touchdown and (2) main stance phase. The reaction time was defined as the time from moment of release to the moment the midpoint of the foot exceeded an acceleration of 1.5 m/s/s. The ground reaction force of both legs was collected using four Kistler force plates at a sampling rate of 1080 Hz. At the beginning of each trial subjects stood on two force plates and when the fall was induced they used a one step strategy and stepped forward onto another force plate. Ground reaction forces of both feet were inspected before each ‘fall’ to confirm that subjects were standing symmetrically with their weight evenly distributed between their right and left legs. The margin of stability in the anteroposterior direction was calculated according to Hof et al. (2005) as follows:
V XCM bx ¼ U x max X CM ; where X CM ¼ PXCM þ pffiffiffiffiffiffiffi g=l bx is the margin of stability in the anteroposterior direction, U x max is the anterior boundary of the base of support (i.e. horizontal component of the projection of the toe from the recovery limb to the ground; a zero value represents the position of the toe before release), and X CM is the position of the extrapolated CM in the anteroposterior direction. P XCM is the horizontal (anteroposterior) component of the projection of the CM to the ground, V XCM is the horizontal (anteroposterior) CM velocity, g is the acceleration of gravity, and l is the distance between CM and centre of the ankle p joint in the sagittal plane. The term g/l is known as the eigenfrequency. Hof et al. (2005) used the eigenfrequency for much smaller angles, but more recently it has also been shown valid for larger angles of the inverted pendulum (Arampatzis et al., 2008; Curtze et al., 2010; Hof, 2008; Hof et al., 2007). The eigenfrequency is used to calculate the extrapolated center of mass, which tells us where the base of support needs to be to attain stability in a moving (falling) subject. Postural stability is maintained in circumstances where the position of the extrapolated CM is within the base of support (positive values of margin of stability) while stability is lost in cases where the extrapolated CM surpasses the anterior boundary of the base of support. 4. Statistics Paired T-tests were performed to determine pre-fatigue/postfatigue differences in the components of dynamic stability at both touchdown and minimum knee angle. Additionally, paired t-tests were used to compare, the margin of stability, the maximum hip,
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knee and ankle joint torques, reaction time and time to touchdown, maximum vertical and horizontal forces, and time to joint torques between the pre and post measurements. For this study differences were considered significant if p 6 0.05. No differences in the results were found regarding subject height 5. Results
Table 2 Kinematic and kinetic parameters during the main stance phase means ± SD minimum knee joint angle of the recovery limb after touchdown (Knee anglemin), duration of the main stance phase, average of vertical and horizontal ground reaction forces (Average GRFvertical, Average GRFhorizontal), vertical and horizontal force integral over time (vertical force integral, horizontal force integral) and resultant joint moments, maximum moment at the ankle (Max momentankle), knee (Max momentknee) and Hip (Max momenthip) joints, of the recovery limb during the main phase, Boundary of base of support, extrapolated centre of mass, projected centre of p mass, centre of mass velocity, g/l at minimum knee angle of the stance phase.
5.1. Fatigue protocol
5.2. Phase until touchdown Although the reaction time showed a slight increase after the fatigue protocol compared to the non-fatigued value, the difference was insignificant (p > 0.05) (Table 1). The fatigue protocol had no effect on duration until touchdown (Table 1). Results of the dependent T-tests showed no significant changes (p > 0.05) in the anterior boundary of the base of support, horizontal component of the projection pffiffiffiffiffiffiffi of the CM to the ground, horizontal CM velocity, the term g=l or the extrapolated centre of mass between the
Table 1 Duration and kinetic parameters at phase until touchdown means ± SD of reaction time, duration until touchdown, maximum of vertical and horizontal ground reaction forces (Max GRFvertical, Max GRFhorizontal) of both legs in the phase until touchdown and maximum moment at the ankle (Max momentankle), knee (Max momentknee) and Hip (Max momenthip) joints of the support limb, Boundary of base of support at touchdown, extrapolated centre of mass at touchdown, projected centre of mass at p touchdown, centre of mass velocity at touchdown and g/l at touchdown. None of the pre-post differences were significant. Parameter
Pre-fatigue
Post-fatigue
Reaction time (ms) Duration until touchdown (ms) Max GRFvertical (N/kg) Max GRFhorizontal (N/kg) Max momentankle (Nm/kg) Max momentknee (Nm/kg) Max momenthip (Nm/kg) Boundary of base of support (cm) Extrapolated centre of mass (cm) Projected cenre of mass (cm) Centre of mass velocity (m/s) p g/l
104 ± 25 405 ± 47 11.71 ± 1.07 6.86 ± 0.93 1.36 ± 0.28 1.13 ± 0.29 0.99 ± 0.49 1.07 ± 0.16 1.05 ± 0.14 0.67 ± 0.08 1.34 ± 0.21 3.67 ± 0.21
121 ± 53 410 ± 51 11.59 ± 1.66 6.73 ± 0.75 1.43 ± 0.33 1.03 ± 0.39 0.82 ± 0.63 1.06 ± 0.13 1.04 ± 0.15 0.67 ± 0.09 1.35 ± 0.27 3.66 ± 0.27
*
Pre-fatigue
Post-fatigue
Knee anglemin (°) Duration main stance phase (ms)* Average GRFvertical (N/kg)* Average GRFhorizontal (N/kg)* Vertical force integral (N s/kg)* Horizontal force integral (N s/kg) Max momentankle (Nm/kg)* Max momentknee (Nm/kg)* Max momenthip (Nm/kg) Boundary of base of support (cm) Extrapolated centre of mass (cm) Projected centre of mass (cm) Centre of mass velocity (m/s) p g/l
112 ± 14 253 ± 75 14.87 ± 1.17 3.79 ± 1.17 3.76 ± 0.77 0.90 ± 0.24 2.17 ± 0.63 1.76 ± 0.58 4.49 ± 1.77 1.07 ± 0.16 0.99 ± 0.14 0.86 ± 0.11 0.52 ± 0.32 3.85 ± 0.85
96 ± 24 340 ± 85 13.28 ± 3.28 2.72 ± 0.95 4.47 ± 1.18 0.84 ± 0.24 1.74 ± 0.37 1.54 ± 0.66 4.19 ± 1.32 1.04 ± 0.14 1.00 ± 0.20 0.91 ± 0.21 0.35 ± 0.30 3.90 ± 0.18
Statistically significant fatigue effect (p < 0.05).
pre and post-fatigue conditions at the instant of touchdown (Table 2). Likewise no significant difference (p > 0.05) was calculated between the pre and post margin of stability at touchdown (Fig. 1). The complete ground reaction force curves of the support and recovery legs can be seen in Fig. 2. The complete joint moment curves for both the support and recovery legs can be seen in Fig. 3. The maximum values of the hip knee and ankle joint moments of the support leg as well as the maximum values for the horizontal and vertical ground reaction force did not differ significantly (p > 0.05) between fatigued and non-fatigued conditions in the phase until touchdown (Table 1). 5.3. Main stance phase The components of dynamic stability control showed no significant differences (p > 0.05) between the pre and post-fatigue conditions during the main stance phase (Table 2). Likewise, no significant difference (p > 0.05) was calculated between the pre and post margin of stability during the main stance phase (Fig. 1). The duration of the main stance phase after the fatigue was significantly (p < 0.05) greater compared to the non-fatigued
40
Pre
Post
30
Margin of Stability [cm]
Subjects performed the 4 sets of fatiguing dynamic squats lasting 104 ± 43, 61 ± 21, 57 ± 29, 44 ± 15 s, respectively. Because the tempo of the fatiguing squats varied with state of fatigue, the researcher decided to report the times of the trials. Since the subjects were not allowed to rest at the top, the reported times are approximately the amount of time the lower extremity of the subjects were being loaded during each set. The results of the pre and post isometric squats showed a decrease in the maximum voluntary squat induced by the fatigue protocol. The Isometric squat maximums for the group of subjects before and directly after the fatigue protocol were 27.3 ± 9.5 N/kg body mass and 21.0 ± 7.0 N/kg body mass. This was a reduction of 23 ± 8% of the original maximum. After the last dynamic stability test the isometric maximum recovered to 18 ± 9% of the original maximum value (22.4 ± 9.2 N/kg). The final dynamic stability test was after the 2nd isometric max and before the 3rd isometric max indicating that the fatigue experience by the subjects at the time of the post dynamic stability test was between 77% and 82% of their maximum. At release during the forward falls, the margin of stability did not show any significant differences between the pre and post-fatigue condition (pre: 32.1 ± 5.6 cm, post: 32.0 ± 6.8 cm) indicating that the participants started the falls from the same incline position.
Parameter
20 10 0 -10 -20 -30
TD
END
TD
END
Fig. 1. Individual and mean (SD) values of margin of stability for the pre and post conditions at the instant of touchdown (TD) and at the end of the main stance phase (end).
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Release
TD
Release Pre 6 Post
END
FX (N/kg)
FX (N/kg)
3 0 -3 -6
Pre Post
-9
2
8 FZ (N/kg)
20 FZ (N/kg)
4
0
25
15 10 5 0
TD
0
200
400 600 Time (ms)
6 4 2 0
800
0
100
200 Time (ms)
300
400
Fig. 2. Mean and SEM curves of the horizontal (Fx) and vertical (Fz) ground reaction force of the recovery leg (left) from release until 800 ms after touchdown and of the support leg (right) from release until touchdown before (pre) and after (post) the fatiguing task.
Release
END
Dorsal
-1 -2
2
Plantar Extension
Knee (Nm/kg)
-3 3
1 0 -1 2
Hip (Nm/kg)
TD
Ankle (Nm/kg)
0
Release
Flexion Flexion
Hip (Nm/kg)
Knee (Nm/kg)
Ankle (Nm/kg)
1
0 -2 -4 -6 Extension 0 200
0 -1
800
Pre Post
-2
Plantar Extension
0 -1 -2
Flexion
1
Flexion
0 -1 -2
400 600 Time (ms)
TD Dorsal
Extension
0
100
200 Time (ms)
300
400
Fig. 3. Mean and SEM curves of the sagittal plane joint moments (internal) of the ankle, knee and hip joints of the recovery leg (left) from release until 800 ms after touchdown and of the support leg (right) from release until touchdown before (pre) and after (post) the fatiguing task.
condition (Table 2). In the fatigued condition, the participant’s minimum lead leg knee angle went into significantly more flexion during the main stance phase leading to an increased increment in time available to decelerate the horizontal CM motion. The average horizontal and vertical forces of the recovery leg decreased significantly with fatigue (Table 2). Although the average horizontal force decreased, the increase in time led to the same horizontal force integral of the recovery leg (Table 2). After the fatiguing protocol the participants did not show any differences in the maximal hip joint moment of the recovery leg during the main stance phase compared to the unfatigued condition (Table 2). At the ankle and
knee joints the maximal moment values were lower after the fatigue than before (Table 2).
6. Discussion The purpose of the present study was to investigate the effect of fatigue of the lower extremity on the dynamic stability control of young adults during forward falls. The fatigue related decrease in muscle strength induced by our fatigue protocol did not affect the margin of stability, the horizontal component of the projection
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of the CM, the boundaries p offfiffiffiffiffiffi the ffi base of support, the horizontal CM-velocity and the term g=l during the forward induced falls. In short, the fatigue caused by our fatiguing protocol did not negatively affect the subject’s dynamic stability control to the extent that the subjects’ ability to prevent falling was impaired. This goes against our hypothesis. Our muscle fatigue induced by repetitive squats appeared to cause a reduction in the force generating capacity of the leg extensors muscles in the post-fatigue test of about 20% as measured by a maximum isometric squat. The motor behaviour of the examined participants was not affected in the phase until touchdown due to the reduction in force generating capacity. In the phase until touch down, the maximum values of the resultant moments at the ankle, knee and hip joints as well as of the ground reaction forces in the post-fatigue condition did not show any differences to the pre-fatigue values in both legs (i.e. support and recovery leg). In a similar manner the increase of the base of support in the phase until touchdown as well as the needed time were equal between the two conditions. The participants were able to attain the same boundary of the base of support at the same velocity and thus the same margin of stability at touchdown as in the non-fatigued condition despite of the reduced force generation capacity of the leg extensors. An explanation of this phenomenon may be the relative lower resultant joint moment values needed during the phase until touchdown compared to the main stance phase. This means that the main mechanism (i.e. increased base of support in relation to extrapolated CM) during the forward falls to regain balance does not require high level joint moments and thus high level muscle forces from the human system. Furthermore, the fact that all participants who showed positive values in margin of stability at touchdown achieved a stable position in the end of the main phase indicates that the state of stability at touchdown determines the ability of the human system to recover balance with a single step after forwards falls. Therefore the ability of the participants to increase the base of support in relation to extrapolated CM during the phase until touchdown seems to be the most important event for dynamic stability control after sudden induced forward falls. One alternate hypothesis is that fatigued hip flexors would impair the ability to regain balance during a forward fall. This alternate hypothesis is supported by the fact that successful balance recovery was based on the margin of stability at touchdown. In other words, if they got their foot out far enough in front of them, they were able to stop their fall and regain balance. Because they are falling the amount of time to place their lead foot out in front of them is limited. Therefore it seems plausible the ability to quickly flex at the hip, likely influenced by hip flexor strength, may be a deciding factor in achieving an acceptable margin of stability and regaining balance during forward falls. Knee flexion and ankle dorsiflexion could possibly also help recovery by shortening the moment arms of the leg around the hip joint and aiding in toe clearance. These findings have important implications for interventions strategies to prevent falls during daily life. It is accepted that muscle strength and tendon stiffness contribute significantly (30– 40%) to the capacity of the human system to regain balance after forward falls (Wojcik et al., 2001; Grabiner et al., 2005; Karamanidis and Arampatzis, 2007; Karamanidis et al., 2008). Our results indicate that increased strength of the lower extremity extensors may not be the only effective intervention strategy for preventing falls. The ability of humans to immediately generate proper motor behaviour for successful postural corrections including mechanisms responsible to maintain stability seems to be very important for fall preventions. Increasing the base of support after a perturbation does not require high levels of muscle force. Therefore, we can argue that, practicing motor tasks including mechanisms responsible for dynamic stability control, such as a quick lunge step, may
contribute in an improvement in the ability to recover balance without falling. During the main stance phase several significant modifications in the way to achieve balance were documented indicating that the fatiguing protocol did affect certain aspects of the dynamic stability control. The decrease in the maximum ankle and knee joint moments during the main stance phase show that the fatiguing protocol affected the moment generation in the lower extremities joints. As a consequence the horizontal and vertical ground reaction forces decreased during the main stance phase after the fatigue. Nevertheless, the participants showed similar margins of stability in the end of the main stance phase in the pre- and post-fatigue conditions. They were able to counteract the decreased average horizontal ground reaction forces after the fatigue by flexing their lead leg knee to a greater extent thereby increasing the deceleration time of the horizontal CM velocity. This adjustment in the recovery leg resulted to similar integral of the horizontal ground reaction force during the main stance as that in nonfatigued condition. The results indicate an appropriate adjustment of the human system to compensate for the deficit in muscle strength. The concept of the extrapolated centre of mass used in the current study is based on the inverted pendulum model. Although the formulation has been progressed from standing balance to dynamic conditions (i.e. when CM has an initial velocity) the model is a simplification of the human body as a pendulum with a mass (Arampatzis et al., 2008; Hof, 2008; Hof et al., 2007, 2005; Curtze et al., 2010). During dynamic situations, for example the simulated forward falls, several segments of the human body are moving around the CM. The non consideration of these movements in the model may reveal some inaccuracies regarding the state of stability. Another limitation is that because our fatigue protocol used a multi-joint exercise performed to self determined exhaustion the exact fatigue level of any of the given muscles is unknown. We believe that this loss of control was justified by the increase in ecological validity of the dynamic squat exercise over, for example, an isometric leg extension. We concluded that the decrease in lower extremity extensor muscle strength after the fatiguing submaximal contractions did not lead to functional deficits related to the capacity of the human system to regain balance after forward induced falls. This demonstrates that this specific impairment of the musculoskeletal system alone cannot predict the postural performance. The main mechanism responsible for regaining balance after a forward fall from a forward inclined position is increasing the base of support during the swing phase of the recovery limb and the using of this mechanism does not require high level muscle forces from the humans. We suggested that exercise interventions including mechanisms responsible for dynamic stability control may allow humans to learn and effectively use these mechanisms during sudden perturbations and, hence, reduce the risk of falls during daily life. References Arampatzis A, Karamanidis K, Mademli L. Deficits in the way to achieve balance related to mechanisms of dynamic stability control in the elderly. J Biomech 2008;41:1754–61. Curtze C, Hof AL, Otten B, Postema K. Balance recovery after an evoked forward fall in unilateral transtibial amputees. Gait Posture 2010;3:336–41. Grabiner MD, Owings TM, Pavol MJ. Lower extremity strength plays only a small role in determining the maximum recoverable lean angle in older adults. J Gerontol A-Biol Sci Med Sci 2005;60:M1447–50. Granacher U, Zahner L, Gollhofer G. Strength, power, and postural control in seniors; considerations for functional adaptations and for fall prevention. Eur J Sports Sci 2008;8(6):325–40. Hof AL. The equations of motion for a standing human reveal three mechanisms for balance. J Biomech 2007;40:451–7. Hof AL. The ‘extrapolated center of mass’ concept suggests a simple control of balance in walking. Hum Mov Sci 2008;27:112–25.
M. Walsh et al. / Journal of Electromyography and Kinesiology 21 (2011) 270–275 Hof AL, Gazendam MG, Sinke WE. The condition for dynamic stability. J Biomech 2005;38:1–8. Hof AL, van Bockel RM, Schoppen T, Postema K. Control of lateral balance in walking, experimental findings in normal subjects and above-knee amputees. Gait Posture 2007;25:250–8. Hsiao ET, Robinovitch SN. Biomechanical influences on balance recovery by stepping. J Biomech 1999;32:1099–106. Karamanidis K, Arampatzis A. Age-related degeneration in leg extensor muscletendon units decreases recovery performance after a forward fall: compensation with running experience. Eur J Appl Physiol 2007;99:73–85. Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol 2008;18:980–9. Mademli Lida, Arampatzis Adamantios, Karamanidis Kiros. Dynamic stability control in forward falls: postural corrections after muscle fatigue in young and older adults. Eur J Appl Physiol 2008;103(3):295–306. Madigan, M.L., Lloyd, E.M., Age related differences in peak joint torquesduring the support phase of single step recovery from a forward fall. J Gerontol A-Biol Sci Med Sci 2005;60:910–4. Moritani T, Oddson L, Thorstensson A. Electromyographic evidence of selective fatigue during the eccentric phase stretch/shortening cycles in man. Eur J Appl Physiol 1990(60):425–9. Pijnappels M, Bobbert MF, van Dieen JH. Push-off reactions in recovery after tripping discriminate young subjects, older non-fallers and older fallers. Gait Posture 2005;21:388–94. Simoneau M, Corbeil P. The effect of time to peak ankle torque on balance stability boundary: experimental validation of a biomechanical model. Exp Brain Res 2005;165:217–28. Thelen DG, Wojcik LA, Schultz AB, Ashton-Miller JA, Alexander NB. Age differences in using a rapid step to regain balance during a forward fall. J Gerontol A-Biol Sci Med Sci 1997;52(1):M8–M13. Wojcik LA, Thelen DG, Schultz AB, Ashton-Miller JA, Alexander NB. Age and gender differences in peak lower extremity joint torques and ranges of motion used during single-step balance recovery from a forward fall. J Biomech 2001;34(1):67–73. Yeung SS, Au AL, Chow CC. Effects of Fatigue on the temporal neuromuscular control of the vastus medialis muscles in humans. Eur J Appl Physiol 1999;8:379–85. Zatsiorsky VM, Selujanov VN. The mass and inertia characteristics of the main segments of the human body. In: Matsui H, Kabayashi K, editors. Biomechanics VIIIB. Champaign, IL: Human Kinetics; 1983. pp. 1152–9.
Mark Walsh is an associate professor at Miami University in the United States. He received his Ph.D. in biomechanics at the German Sport University Cologne, Germany. His research interests include the mechanics of human movement, balance and sport biomechanics.
Andreas Peper graduated in sport science at the German Sport University of Cologne. There he started his Ph.D. in the field of dynamic stability control of elderly persons in conjunction with different training interventions and continues his thesis since May 2009 at the department of training and movement science of the Humboldt-University of Berlin.
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Stefanie Bierbaum graduated 2006 in sport science at the German Sport University of Cologne. She started her Ph.D. in biomechanics at the Institute for Biomechanics of the German Sport University and continues with her work since 2009 at the department of training and movement science of the Humboldt-University of Berlin. She is doing her Ph.D. thesis on locomotor adaptation (short- and long-term) and dynamic stability of the elderly.
Kiros Karamanidis, received his Ph.D. at the German Sport University of Cologne in 2006. His main research interests are in the field of adaptation of aging muscles and its effect on gait mechanics focusing on the prevention of falls in the elderly.
Adamantios Arampatzis is professor and chair of the Department Training and Movement Sciences at the Humboldt-University of Berlin. Among his research interests are the plasticity of the musculoskeletal system to exercise and the influence of the neuromuscular capacity of the human system on motor task behaviour during daily and sport activities. His research work concentrates on muscle–tendon unit adaptation, neuromuscular control of locomotion, dynamic stability and joint mechanics.
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Effects of submaximal fatiguing contractions on the components of dynamic stability control after forward falls Mark Walsh a,⇑, Andreas Peper b,c, Stefanie Bierbaum b,c, Kiros Karamanidis c, Adamantios Arampatzis b a
Department of Kinesiology and Health, Miami University, Oxford, OH 45056, USA Department of Training and Movement Sciences, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 11, 10115 Berlin, Germany c Institute of Biomechanics and Orthopaedics, German Sport University Cologne, Carl-Diem-Weg 6, D-50933 Cologne, Germany b
a r t i c l e
i n f o
Article history: Received 5 February 2010 Received in revised form 7 December 2010 Accepted 10 December 2010
Keywords: Margin of stability Falling Fatigue Muscle strength
a b s t r a c t The present study aimed to investigate the effect of lower extremity muscle fatigue on the dynamic stability control of physically active adults during forward falls. Thirteen participants (body mass: 70.2 kg, height: 175 cm) were instructed to regain balance with a single step after a sudden induced fall from a forward-leaning position before and after the fatigue protocol. The ground reaction forces were collected using four force plates at a sampling rate of 1080 Hz. Kinematic data were recorded with 12 vicon cameras operating at 120 Hz. Neither the reaction time nor the duration until touchdown showed any differences (p > 0.05). The ability of the subjects to prevent falling did not change after the fatigue protocol. In the fatigued condition, the participants demonstrated an increase in knee flexion during the main stance phase and an increased time to decelerate the horizontal CM motion (both p < 0.05). Significant (p < 0.05) decreases were seen post-fatigue in average horizontal and vertical force and maximum knee and ankle joint moments. The fatigue related decrease in muscle strength did not affect the margin of stability, the boundary of the base of support or the position of the extrapolated centre of mass during the forward induced falls, indicating an appropriate adjustment of the motor commands to compensate the deficit in muscle strength. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Falls are an inherent part of life for most everyone. A number of factors may contribute to falls. Many studies have examined static and dynamic balance situations in an attempt to learn more about how the human system controls stability and prevents falls. Although aging is a common focus of balance literature, a loss of muscular strength can also be induced through means other than aging, such as fatigue (Yeung et al., 1999; Moritani et al., 1990). Several studies reported that loss of muscle strength may alter the capacity of the human system to generate rapid force for balance corrections after sudden perturbations (Granacher et al., 2008; Pijnappels et al., 2005; Simoneau and Corbeil, 2005). Karamanidis and Arampatzis (2007) reported that muscle–tendon capacities of the lower limbs contribute about 33% to balance recovery after forward induced falls. However, postural corrections after a sudden perturbation involve sensorimotor adaptational responses which include mechanisms responsible for maintaining the dynamic stability and thus muscle weakness may be partly compensated for by proper planning and execution of the used locomotion strategy. By using fatigued younger subjects to test
⇑ Corresponding author. Tel.: +1 513 529 2708; fax: +1 513 529 5006. E-mail address: [email protected] (M. Walsh). 1050-6411/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2010.12.005
the effects of muscular strength on forward falls we can control for the other changes that occur with aging. Three mechanisms have been presented (Hof, 2007) by which stability may be maintained; by (1) increasing the base of support with relation to the extrapolated centre of mass, (2) counter rotating segments around the CM, and (3) applying an external force other than the ground reaction force (e.g. grasping a handrail or secure object). Examining the human’s capabilities to regain balance after sudden release from a forward inclined body position is a common way to assess dynamic stability (Hsiao and Robinovitch, 1999; Thelen et al., 1997; Wojcik et al., 2001). The margin of stability during locomotion can be quantified by the position of the extrapolated centre of mass (CM) in relation to the base of support (Hof et al., 2005). When the position of the extrapolated CM exceeds the anterior boundary of the base of support, the result is a loss of stability (Hof et al., 2005). Although studies regarding either fatigue or balance are numerous, to date only one study we found has examined the effects of fatigue on dynamic stability control (Mademli et al., 2008). This study found that fatigue had no effect on the components of dynamic stability. However, the fatigue protocol for this study used the knee extension exercise and therefore only fatigued the knee extensor muscles. Preventing a forward fall requires a motion from the front leg that is similar to a lunge and requires not only the knee extensor muscles, but also hip and ankle muscles. The knee extension is a single joint movement requiring
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force production from one muscle group and has little relevance to normal human movement. Additionally, it has been reported that to regain balance during forward falls, extensor muscles from the major lower extremity joints (hip, knee and ankle) are all important (Pijnappels et al., 2005; Madigan and Lloyd, 2005). Therefore the purpose of the present study is to experimentally investigate the effect of fatigue of the lower extremity, induced by submaximal fatiguing contractions, on the dynamic stability control of young adults during forward falls. We hypothesize that dynamic stability will be compromised when the lower extremity is fatigued. This could be seen in a decrease in the ability to regain balance after an induced forward fall.
2. Methods Thirteen participants (7 men and 6 women), age 27.7 ± 4.5 years, body mass: 70.2 ± 13.1 kg, body height: 175 ± 11.1 cm, participated in this study. Before the initiation of this experiment, the procedures were explained to the subjects and informed consent protocol was followed in accordance with the rules of the University Human Subjects Board. Subjects were instructed to regain balance with a single step after a sudden induced fall from a forward-leaning position both before and after a fatiguing protocol targeting the lower extremity. The experiment was performed at the maximal individual lean angle of each participant (maximal forward incline position was where the subjects were able to regain balance with a single step after the sudden release of a support cable which supported them from behind). The force on the cable at maximum lean position was between 25–40% bodyweight. The maximal individual lean angle was determined experimentally before the main experiment. After a short rest (5 min) subjects were tested at their previously measured maximum lean angle. The experimental design of the balance recovery task has been previously described (Karamanidis and Arampatzis, 2007). Following the determination of the subject’s maximum lean angle from which they can be released and still catch themselves, all subjects performed a maximum voluntary isometric squat. Subjects performed the isometric squat with a knee angle of approximately 110 °C. The knee angle was controlled using a goniometer. The isometric squats were performed on a force platform with an adjustable squat bar that was fixed at a height so that the subject’s knee angle was approximately 110 °C. The maximum measured force as measured by the force platform was considered the isometric squat maximum. For the fatigue protocol, subjects were instructed to perform dynamic squats from an extended knee angle of approximately 180 °C to a lower position of approximately 90 °C. The weight used during the fatiguing protocol was 30% of their maximum isometric squat. The dynamic squats were performed with free weights. Once they reached the extended leg position they immediately started moving down again to eliminate the chance of ‘resting’ during the fatigue protocol. Three spotters were present during the fatigue protocol to help the subject with the last repetitions and to help place the bar on the squat rack. The dynamic squat sets were completed until voluntary exhaustion. After 1 min of rest another set of squats was performed and this was repeated until each given subject performed four sets. Directly after the fatigue protocol, the maximum isometric squat of each subject was tested again to measure the extent of the fatigue. Then, immediately after the post maximum isometric squat (30 s) the ability of the subject’s to regain balance with a single step after a sudden induced fall was tested again at their maximum lean angle to see if fatigue affected their dynamic stability control. Following the post induced fall trial, the maximum isometric squat was again tested to document any recovery that may have occurred.
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3. Equipment Kinematic data were tracked using a Vicon Motion Capture System using 12 vicon cameras operating at 120 Hz. Thirty-eight reflective markers (diameter 14 mm) were fixed to landmarks of each subject to aid in motion capture. This included a headband that had four markers on it. The whole body model was used to calculate joint angles, the parameters of dynamic stability and the resultant joint moments through inverse dynamics. We used data provided by Zatsiorsky and Selujanov (1983) to calculate masses and moments of inertia of the body segments. For the trials of each subject, the release, touchdown and minimum knee joint angle were identified. The time of release was defined as the moment the cable holding the subjects in a forward lean was released. Touchdown was defined as the moment the recovery leg contacted the ground after the step. This event was identified using a Kistler force plate (60 90 cm, Kistler, Winterhur, Switzerland, trigger was force exceeding 20 N). Minimum knee angle corresponded with the vertical velocity of the subject reaching a value close to 0 m/s. Using those three points, two recovery phases were identified: (1) phase until touchdown and (2) main stance phase. The reaction time was defined as the time from moment of release to the moment the midpoint of the foot exceeded an acceleration of 1.5 m/s/s. The ground reaction force of both legs was collected using four Kistler force plates at a sampling rate of 1080 Hz. At the beginning of each trial subjects stood on two force plates and when the fall was induced they used a one step strategy and stepped forward onto another force plate. Ground reaction forces of both feet were inspected before each ‘fall’ to confirm that subjects were standing symmetrically with their weight evenly distributed between their right and left legs. The margin of stability in the anteroposterior direction was calculated according to Hof et al. (2005) as follows:
V XCM bx ¼ U x max X CM ; where X CM ¼ PXCM þ pffiffiffiffiffiffiffi g=l bx is the margin of stability in the anteroposterior direction, U x max is the anterior boundary of the base of support (i.e. horizontal component of the projection of the toe from the recovery limb to the ground; a zero value represents the position of the toe before release), and X CM is the position of the extrapolated CM in the anteroposterior direction. P XCM is the horizontal (anteroposterior) component of the projection of the CM to the ground, V XCM is the horizontal (anteroposterior) CM velocity, g is the acceleration of gravity, and l is the distance between CM and centre of the ankle p joint in the sagittal plane. The term g/l is known as the eigenfrequency. Hof et al. (2005) used the eigenfrequency for much smaller angles, but more recently it has also been shown valid for larger angles of the inverted pendulum (Arampatzis et al., 2008; Curtze et al., 2010; Hof, 2008; Hof et al., 2007). The eigenfrequency is used to calculate the extrapolated center of mass, which tells us where the base of support needs to be to attain stability in a moving (falling) subject. Postural stability is maintained in circumstances where the position of the extrapolated CM is within the base of support (positive values of margin of stability) while stability is lost in cases where the extrapolated CM surpasses the anterior boundary of the base of support. 4. Statistics Paired T-tests were performed to determine pre-fatigue/postfatigue differences in the components of dynamic stability at both touchdown and minimum knee angle. Additionally, paired t-tests were used to compare, the margin of stability, the maximum hip,
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knee and ankle joint torques, reaction time and time to touchdown, maximum vertical and horizontal forces, and time to joint torques between the pre and post measurements. For this study differences were considered significant if p 6 0.05. No differences in the results were found regarding subject height 5. Results
Table 2 Kinematic and kinetic parameters during the main stance phase means ± SD minimum knee joint angle of the recovery limb after touchdown (Knee anglemin), duration of the main stance phase, average of vertical and horizontal ground reaction forces (Average GRFvertical, Average GRFhorizontal), vertical and horizontal force integral over time (vertical force integral, horizontal force integral) and resultant joint moments, maximum moment at the ankle (Max momentankle), knee (Max momentknee) and Hip (Max momenthip) joints, of the recovery limb during the main phase, Boundary of base of support, extrapolated centre of mass, projected centre of p mass, centre of mass velocity, g/l at minimum knee angle of the stance phase.
5.1. Fatigue protocol
5.2. Phase until touchdown Although the reaction time showed a slight increase after the fatigue protocol compared to the non-fatigued value, the difference was insignificant (p > 0.05) (Table 1). The fatigue protocol had no effect on duration until touchdown (Table 1). Results of the dependent T-tests showed no significant changes (p > 0.05) in the anterior boundary of the base of support, horizontal component of the projection pffiffiffiffiffiffiffi of the CM to the ground, horizontal CM velocity, the term g=l or the extrapolated centre of mass between the
Table 1 Duration and kinetic parameters at phase until touchdown means ± SD of reaction time, duration until touchdown, maximum of vertical and horizontal ground reaction forces (Max GRFvertical, Max GRFhorizontal) of both legs in the phase until touchdown and maximum moment at the ankle (Max momentankle), knee (Max momentknee) and Hip (Max momenthip) joints of the support limb, Boundary of base of support at touchdown, extrapolated centre of mass at touchdown, projected centre of mass at p touchdown, centre of mass velocity at touchdown and g/l at touchdown. None of the pre-post differences were significant. Parameter
Pre-fatigue
Post-fatigue
Reaction time (ms) Duration until touchdown (ms) Max GRFvertical (N/kg) Max GRFhorizontal (N/kg) Max momentankle (Nm/kg) Max momentknee (Nm/kg) Max momenthip (Nm/kg) Boundary of base of support (cm) Extrapolated centre of mass (cm) Projected cenre of mass (cm) Centre of mass velocity (m/s) p g/l
104 ± 25 405 ± 47 11.71 ± 1.07 6.86 ± 0.93 1.36 ± 0.28 1.13 ± 0.29 0.99 ± 0.49 1.07 ± 0.16 1.05 ± 0.14 0.67 ± 0.08 1.34 ± 0.21 3.67 ± 0.21
121 ± 53 410 ± 51 11.59 ± 1.66 6.73 ± 0.75 1.43 ± 0.33 1.03 ± 0.39 0.82 ± 0.63 1.06 ± 0.13 1.04 ± 0.15 0.67 ± 0.09 1.35 ± 0.27 3.66 ± 0.27
*
Pre-fatigue
Post-fatigue
Knee anglemin (°) Duration main stance phase (ms)* Average GRFvertical (N/kg)* Average GRFhorizontal (N/kg)* Vertical force integral (N s/kg)* Horizontal force integral (N s/kg) Max momentankle (Nm/kg)* Max momentknee (Nm/kg)* Max momenthip (Nm/kg) Boundary of base of support (cm) Extrapolated centre of mass (cm) Projected centre of mass (cm) Centre of mass velocity (m/s) p g/l
112 ± 14 253 ± 75 14.87 ± 1.17 3.79 ± 1.17 3.76 ± 0.77 0.90 ± 0.24 2.17 ± 0.63 1.76 ± 0.58 4.49 ± 1.77 1.07 ± 0.16 0.99 ± 0.14 0.86 ± 0.11 0.52 ± 0.32 3.85 ± 0.85
96 ± 24 340 ± 85 13.28 ± 3.28 2.72 ± 0.95 4.47 ± 1.18 0.84 ± 0.24 1.74 ± 0.37 1.54 ± 0.66 4.19 ± 1.32 1.04 ± 0.14 1.00 ± 0.20 0.91 ± 0.21 0.35 ± 0.30 3.90 ± 0.18
Statistically significant fatigue effect (p < 0.05).
pre and post-fatigue conditions at the instant of touchdown (Table 2). Likewise no significant difference (p > 0.05) was calculated between the pre and post margin of stability at touchdown (Fig. 1). The complete ground reaction force curves of the support and recovery legs can be seen in Fig. 2. The complete joint moment curves for both the support and recovery legs can be seen in Fig. 3. The maximum values of the hip knee and ankle joint moments of the support leg as well as the maximum values for the horizontal and vertical ground reaction force did not differ significantly (p > 0.05) between fatigued and non-fatigued conditions in the phase until touchdown (Table 1). 5.3. Main stance phase The components of dynamic stability control showed no significant differences (p > 0.05) between the pre and post-fatigue conditions during the main stance phase (Table 2). Likewise, no significant difference (p > 0.05) was calculated between the pre and post margin of stability during the main stance phase (Fig. 1). The duration of the main stance phase after the fatigue was significantly (p < 0.05) greater compared to the non-fatigued
40
Pre
Post
30
Margin of Stability [cm]
Subjects performed the 4 sets of fatiguing dynamic squats lasting 104 ± 43, 61 ± 21, 57 ± 29, 44 ± 15 s, respectively. Because the tempo of the fatiguing squats varied with state of fatigue, the researcher decided to report the times of the trials. Since the subjects were not allowed to rest at the top, the reported times are approximately the amount of time the lower extremity of the subjects were being loaded during each set. The results of the pre and post isometric squats showed a decrease in the maximum voluntary squat induced by the fatigue protocol. The Isometric squat maximums for the group of subjects before and directly after the fatigue protocol were 27.3 ± 9.5 N/kg body mass and 21.0 ± 7.0 N/kg body mass. This was a reduction of 23 ± 8% of the original maximum. After the last dynamic stability test the isometric maximum recovered to 18 ± 9% of the original maximum value (22.4 ± 9.2 N/kg). The final dynamic stability test was after the 2nd isometric max and before the 3rd isometric max indicating that the fatigue experience by the subjects at the time of the post dynamic stability test was between 77% and 82% of their maximum. At release during the forward falls, the margin of stability did not show any significant differences between the pre and post-fatigue condition (pre: 32.1 ± 5.6 cm, post: 32.0 ± 6.8 cm) indicating that the participants started the falls from the same incline position.
Parameter
20 10 0 -10 -20 -30
TD
END
TD
END
Fig. 1. Individual and mean (SD) values of margin of stability for the pre and post conditions at the instant of touchdown (TD) and at the end of the main stance phase (end).
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Release
TD
Release Pre 6 Post
END
FX (N/kg)
FX (N/kg)
3 0 -3 -6
Pre Post
-9
2
8 FZ (N/kg)
20 FZ (N/kg)
4
0
25
15 10 5 0
TD
0
200
400 600 Time (ms)
6 4 2 0
800
0
100
200 Time (ms)
300
400
Fig. 2. Mean and SEM curves of the horizontal (Fx) and vertical (Fz) ground reaction force of the recovery leg (left) from release until 800 ms after touchdown and of the support leg (right) from release until touchdown before (pre) and after (post) the fatiguing task.
Release
END
Dorsal
-1 -2
2
Plantar Extension
Knee (Nm/kg)
-3 3
1 0 -1 2
Hip (Nm/kg)
TD
Ankle (Nm/kg)
0
Release
Flexion Flexion
Hip (Nm/kg)
Knee (Nm/kg)
Ankle (Nm/kg)
1
0 -2 -4 -6 Extension 0 200
0 -1
800
Pre Post
-2
Plantar Extension
0 -1 -2
Flexion
1
Flexion
0 -1 -2
400 600 Time (ms)
TD Dorsal
Extension
0
100
200 Time (ms)
300
400
Fig. 3. Mean and SEM curves of the sagittal plane joint moments (internal) of the ankle, knee and hip joints of the recovery leg (left) from release until 800 ms after touchdown and of the support leg (right) from release until touchdown before (pre) and after (post) the fatiguing task.
condition (Table 2). In the fatigued condition, the participant’s minimum lead leg knee angle went into significantly more flexion during the main stance phase leading to an increased increment in time available to decelerate the horizontal CM motion. The average horizontal and vertical forces of the recovery leg decreased significantly with fatigue (Table 2). Although the average horizontal force decreased, the increase in time led to the same horizontal force integral of the recovery leg (Table 2). After the fatiguing protocol the participants did not show any differences in the maximal hip joint moment of the recovery leg during the main stance phase compared to the unfatigued condition (Table 2). At the ankle and
knee joints the maximal moment values were lower after the fatigue than before (Table 2).
6. Discussion The purpose of the present study was to investigate the effect of fatigue of the lower extremity on the dynamic stability control of young adults during forward falls. The fatigue related decrease in muscle strength induced by our fatigue protocol did not affect the margin of stability, the horizontal component of the projection
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of the CM, the boundaries p offfiffiffiffiffiffi the ffi base of support, the horizontal CM-velocity and the term g=l during the forward induced falls. In short, the fatigue caused by our fatiguing protocol did not negatively affect the subject’s dynamic stability control to the extent that the subjects’ ability to prevent falling was impaired. This goes against our hypothesis. Our muscle fatigue induced by repetitive squats appeared to cause a reduction in the force generating capacity of the leg extensors muscles in the post-fatigue test of about 20% as measured by a maximum isometric squat. The motor behaviour of the examined participants was not affected in the phase until touchdown due to the reduction in force generating capacity. In the phase until touch down, the maximum values of the resultant moments at the ankle, knee and hip joints as well as of the ground reaction forces in the post-fatigue condition did not show any differences to the pre-fatigue values in both legs (i.e. support and recovery leg). In a similar manner the increase of the base of support in the phase until touchdown as well as the needed time were equal between the two conditions. The participants were able to attain the same boundary of the base of support at the same velocity and thus the same margin of stability at touchdown as in the non-fatigued condition despite of the reduced force generation capacity of the leg extensors. An explanation of this phenomenon may be the relative lower resultant joint moment values needed during the phase until touchdown compared to the main stance phase. This means that the main mechanism (i.e. increased base of support in relation to extrapolated CM) during the forward falls to regain balance does not require high level joint moments and thus high level muscle forces from the human system. Furthermore, the fact that all participants who showed positive values in margin of stability at touchdown achieved a stable position in the end of the main phase indicates that the state of stability at touchdown determines the ability of the human system to recover balance with a single step after forwards falls. Therefore the ability of the participants to increase the base of support in relation to extrapolated CM during the phase until touchdown seems to be the most important event for dynamic stability control after sudden induced forward falls. One alternate hypothesis is that fatigued hip flexors would impair the ability to regain balance during a forward fall. This alternate hypothesis is supported by the fact that successful balance recovery was based on the margin of stability at touchdown. In other words, if they got their foot out far enough in front of them, they were able to stop their fall and regain balance. Because they are falling the amount of time to place their lead foot out in front of them is limited. Therefore it seems plausible the ability to quickly flex at the hip, likely influenced by hip flexor strength, may be a deciding factor in achieving an acceptable margin of stability and regaining balance during forward falls. Knee flexion and ankle dorsiflexion could possibly also help recovery by shortening the moment arms of the leg around the hip joint and aiding in toe clearance. These findings have important implications for interventions strategies to prevent falls during daily life. It is accepted that muscle strength and tendon stiffness contribute significantly (30– 40%) to the capacity of the human system to regain balance after forward falls (Wojcik et al., 2001; Grabiner et al., 2005; Karamanidis and Arampatzis, 2007; Karamanidis et al., 2008). Our results indicate that increased strength of the lower extremity extensors may not be the only effective intervention strategy for preventing falls. The ability of humans to immediately generate proper motor behaviour for successful postural corrections including mechanisms responsible to maintain stability seems to be very important for fall preventions. Increasing the base of support after a perturbation does not require high levels of muscle force. Therefore, we can argue that, practicing motor tasks including mechanisms responsible for dynamic stability control, such as a quick lunge step, may
contribute in an improvement in the ability to recover balance without falling. During the main stance phase several significant modifications in the way to achieve balance were documented indicating that the fatiguing protocol did affect certain aspects of the dynamic stability control. The decrease in the maximum ankle and knee joint moments during the main stance phase show that the fatiguing protocol affected the moment generation in the lower extremities joints. As a consequence the horizontal and vertical ground reaction forces decreased during the main stance phase after the fatigue. Nevertheless, the participants showed similar margins of stability in the end of the main stance phase in the pre- and post-fatigue conditions. They were able to counteract the decreased average horizontal ground reaction forces after the fatigue by flexing their lead leg knee to a greater extent thereby increasing the deceleration time of the horizontal CM velocity. This adjustment in the recovery leg resulted to similar integral of the horizontal ground reaction force during the main stance as that in nonfatigued condition. The results indicate an appropriate adjustment of the human system to compensate for the deficit in muscle strength. The concept of the extrapolated centre of mass used in the current study is based on the inverted pendulum model. Although the formulation has been progressed from standing balance to dynamic conditions (i.e. when CM has an initial velocity) the model is a simplification of the human body as a pendulum with a mass (Arampatzis et al., 2008; Hof, 2008; Hof et al., 2007, 2005; Curtze et al., 2010). During dynamic situations, for example the simulated forward falls, several segments of the human body are moving around the CM. The non consideration of these movements in the model may reveal some inaccuracies regarding the state of stability. Another limitation is that because our fatigue protocol used a multi-joint exercise performed to self determined exhaustion the exact fatigue level of any of the given muscles is unknown. We believe that this loss of control was justified by the increase in ecological validity of the dynamic squat exercise over, for example, an isometric leg extension. We concluded that the decrease in lower extremity extensor muscle strength after the fatiguing submaximal contractions did not lead to functional deficits related to the capacity of the human system to regain balance after forward induced falls. This demonstrates that this specific impairment of the musculoskeletal system alone cannot predict the postural performance. The main mechanism responsible for regaining balance after a forward fall from a forward inclined position is increasing the base of support during the swing phase of the recovery limb and the using of this mechanism does not require high level muscle forces from the humans. We suggested that exercise interventions including mechanisms responsible for dynamic stability control may allow humans to learn and effectively use these mechanisms during sudden perturbations and, hence, reduce the risk of falls during daily life. References Arampatzis A, Karamanidis K, Mademli L. Deficits in the way to achieve balance related to mechanisms of dynamic stability control in the elderly. J Biomech 2008;41:1754–61. Curtze C, Hof AL, Otten B, Postema K. Balance recovery after an evoked forward fall in unilateral transtibial amputees. Gait Posture 2010;3:336–41. Grabiner MD, Owings TM, Pavol MJ. Lower extremity strength plays only a small role in determining the maximum recoverable lean angle in older adults. J Gerontol A-Biol Sci Med Sci 2005;60:M1447–50. Granacher U, Zahner L, Gollhofer G. Strength, power, and postural control in seniors; considerations for functional adaptations and for fall prevention. Eur J Sports Sci 2008;8(6):325–40. Hof AL. The equations of motion for a standing human reveal three mechanisms for balance. J Biomech 2007;40:451–7. Hof AL. The ‘extrapolated center of mass’ concept suggests a simple control of balance in walking. Hum Mov Sci 2008;27:112–25.
M. Walsh et al. / Journal of Electromyography and Kinesiology 21 (2011) 270–275 Hof AL, Gazendam MG, Sinke WE. The condition for dynamic stability. J Biomech 2005;38:1–8. Hof AL, van Bockel RM, Schoppen T, Postema K. Control of lateral balance in walking, experimental findings in normal subjects and above-knee amputees. Gait Posture 2007;25:250–8. Hsiao ET, Robinovitch SN. Biomechanical influences on balance recovery by stepping. J Biomech 1999;32:1099–106. Karamanidis K, Arampatzis A. Age-related degeneration in leg extensor muscletendon units decreases recovery performance after a forward fall: compensation with running experience. Eur J Appl Physiol 2007;99:73–85. Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol 2008;18:980–9. Mademli Lida, Arampatzis Adamantios, Karamanidis Kiros. Dynamic stability control in forward falls: postural corrections after muscle fatigue in young and older adults. Eur J Appl Physiol 2008;103(3):295–306. Madigan, M.L., Lloyd, E.M., Age related differences in peak joint torquesduring the support phase of single step recovery from a forward fall. J Gerontol A-Biol Sci Med Sci 2005;60:910–4. Moritani T, Oddson L, Thorstensson A. Electromyographic evidence of selective fatigue during the eccentric phase stretch/shortening cycles in man. Eur J Appl Physiol 1990(60):425–9. Pijnappels M, Bobbert MF, van Dieen JH. Push-off reactions in recovery after tripping discriminate young subjects, older non-fallers and older fallers. Gait Posture 2005;21:388–94. Simoneau M, Corbeil P. The effect of time to peak ankle torque on balance stability boundary: experimental validation of a biomechanical model. Exp Brain Res 2005;165:217–28. Thelen DG, Wojcik LA, Schultz AB, Ashton-Miller JA, Alexander NB. Age differences in using a rapid step to regain balance during a forward fall. J Gerontol A-Biol Sci Med Sci 1997;52(1):M8–M13. Wojcik LA, Thelen DG, Schultz AB, Ashton-Miller JA, Alexander NB. Age and gender differences in peak lower extremity joint torques and ranges of motion used during single-step balance recovery from a forward fall. J Biomech 2001;34(1):67–73. Yeung SS, Au AL, Chow CC. Effects of Fatigue on the temporal neuromuscular control of the vastus medialis muscles in humans. Eur J Appl Physiol 1999;8:379–85. Zatsiorsky VM, Selujanov VN. The mass and inertia characteristics of the main segments of the human body. In: Matsui H, Kabayashi K, editors. Biomechanics VIIIB. Champaign, IL: Human Kinetics; 1983. pp. 1152–9.
Mark Walsh is an associate professor at Miami University in the United States. He received his Ph.D. in biomechanics at the German Sport University Cologne, Germany. His research interests include the mechanics of human movement, balance and sport biomechanics.
Andreas Peper graduated in sport science at the German Sport University of Cologne. There he started his Ph.D. in the field of dynamic stability control of elderly persons in conjunction with different training interventions and continues his thesis since May 2009 at the department of training and movement science of the Humboldt-University of Berlin.
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Stefanie Bierbaum graduated 2006 in sport science at the German Sport University of Cologne. She started her Ph.D. in biomechanics at the Institute for Biomechanics of the German Sport University and continues with her work since 2009 at the department of training and movement science of the Humboldt-University of Berlin. She is doing her Ph.D. thesis on locomotor adaptation (short- and long-term) and dynamic stability of the elderly.
Kiros Karamanidis, received his Ph.D. at the German Sport University of Cologne in 2006. His main research interests are in the field of adaptation of aging muscles and its effect on gait mechanics focusing on the prevention of falls in the elderly.
Adamantios Arampatzis is professor and chair of the Department Training and Movement Sciences at the Humboldt-University of Berlin. Among his research interests are the plasticity of the musculoskeletal system to exercise and the influence of the neuromuscular capacity of the human system on motor task behaviour during daily and sport activities. His research work concentrates on muscle–tendon unit adaptation, neuromuscular control of locomotion, dynamic stability and joint mechanics.