1 Fabio Augusto Barbieri Impact of muscle fatigue on mechanics and motor control of walking Rio Claro 2012 GRADUATE PROGRAM IN CIÊNCIAS DA MOTRICIDADE UNIVERSIDADE ESTADUAL PAULISTA “JÚLIO DE MESQUITA FILHO” INSTITUTO DE BIOCIÊNCIAS - RIO CLARO 2 FABIO AUGUSTO BARBIERI Impact of muscle fatigue on mechanics and motor control of walking Thesis submitted in partial fulfillment of the requirements of the Instituto de Biociências do Campus de Rio Claro, Universidade Estadual Paulista Júlio de Mesquita Filho, for the degree of Ph.D. in Ciências da Motricidade. Supervisor: Lilian Teresa Bucken Gobbi, Ph.D. Rio Claro 2012 Barbieri, Fabio Augusto Impact of muscle fatigue on mechanics and motor control of walking / Fabio Augusto Barbieri. - Rio Claro : [s.n.], 2012 94 f. : il., figs., tabs. Tese (doutorado) - Universidade Estadual Paulista, Instituto de Biociências de Rio Claro Orientador: Lilian Teresa Bucken Gobbi 1. Cinesiologia. 2. Comportamento morto. 3. Controle motor. 4. Locomoção. 5. Fadiga muscular. 6. Envelhecimento. 7. Nível de atividade física. I. Título. 796.022 B236i Ficha Catalográfica elaborada pela STATI - Biblioteca da UNESP Campus de Rio Claro/SP 3 FABIO AUGUSTO BARBIERI Impact of muscle fatigue on mechanics and motor control of walking Thesis submitted in partial fulfillment of the requirements of the Instituto de Biociências do Campus de Rio Claro, Universidade Estadual Paulista Júlio de Mesquita Filho, for the degree of Ph.D. in Ciências da Motricidade. Defense committee Jaap H. van Dieën, Ph.D. Lilian Teresa Bucken Gobbi, Ph.D. Luis Mochizuki, Ph.D. Quincy Almeida, Ph.D. Renato de Moraes, Ph.D. Rio Claro, 28 de Novembro de 2012. 4 “Always overcoming challenges and goals” i 5 I dedicate this thesis to my family and the special friends of my life. ii 6 ACKNOWLEDGEMENTS I appreciate CAPES, FAPESP and FUNDUNESP for financial support. I would like to thank everyone that helped in this thesis. Specially, I would like to thank: - My supervisor Dr. Lilian Teresa Bucken Gobbi for the opportunity to develop my Ph.D and to encourage me braking barriers; - The defense committee for the ideas and comments. Specially, Dr. Jaap H. van Dieën, who gave me the opportunity to develop part of Vrije University Amsterdam and improved so much my knowledge; - The members of LEPLO, Posture and Gait Studies Laboratory, for the acquaintanceship; - Dr. Mirjam Pijnappels, Dr. Yun Ju Lee, MSc. Marit Balder, Ms. Rodrigo Vitório, MSc. Ellen Lirani Silva, MSc. Claudia Teixeira Arroyo, Paulo Cezar Rocha dos Santos, Lucas Simieli, Diego Orcioli Silva, and André Maccari for helping to collect data and intellectual advices. iii 7 ABSTRACT The aim of the study is to analyze the effects of muscle fatigue on mechanics and motor control of walking in different environments. A series of walking experiments addressedmuscle fatigue impact in different gait tasks, age-related changes in control of gait with muscle fatigue, and effects of fatigue in different muscular group on mechanics and control of gait during stepping down. The present thesis showed that quadriceps muscle fatigue modifies gait fairly independent of the environment. In walking on a level surface, during obstacle crossing and during stepping down quadriceps fatigue caused with a wider basis of support and reduced stride duration, but without modulation of placement of the feet in crossing an obstacle and stepping down a curb. This strategyimproves the balance to avoid falling. Furthermore, the mechanics and control during the last stride before stepping down and in landing phase were dependent on whether ankle muscles or knee muscles were fatigued. It should be noted that the joint used to absorb kinetic energy in stepping down with ankle muscle fatigue was dependent on whether a heel or toe landing strategy was used. However, the variability of trailing and leading foot-step horizontal distance was higher after both fatigue protocols, which indicates a reduced control of foot placement. Moreover, the effects of knee muscle fatigue on even and uneven walking of young adults were independent of physical activity level but age-related. The spatial-temporal and kinetic modulations in both tasks after knee muscle fatigue started over 40 years old with a risky strategy for older individuals (over 60 years old). In conclusion: a) knee muscle fatigue affects medio-lateral balance control independently of type of gait, which were compensated by modulation of the spatial-temporal and kinetic parameters, angular movement, muscle activity and energy absorption to maintain stability; b) compensatory muscle strategies were used according to the muscle groups that were fatigued, recruiting unfatigued muscle groups to adjust the gait pattern and to enhance balance control. In addition, the variability of trailing and leading foot- step horizontal distances increased with fatigue, suggesting a loss of control; c) physical activity level did not mediate the effects of knee muscle fatigue on walking on even and uneven surfaces in young adults. On the other hand, the aging process impacts the walking over even and uneven terrains after knee muscles fatigue. Key-words: Muscle fatigue; Walking; Obstacle; Stepping down; Aging; Physical activity level; Biomechanics; Motor control. iv 8 RESUMO O objetivo do estudo é analisar os efeitos da fadiga muscular na mecânica e controle motor do andar em diferentes ambientes. Uma série de estudos envolvendo fadiga e andar analisaram o impacto da fadiga no andar em diferentes ambientes, as mudanças no controle do andar relacionado com a fadiga muscular, e os efeitos da fadiga em diferentes grupos musculares na mecânica e controle do andar durante descida de degrau. A presente tese mostrou que a fadiga no quadríceps modifica substancialmente o padrão do andar independentemente do ambiente. No andar em ambiente regular, durante a ultrapassagem de obstáculo e durante a descida de obstáculo, a fadiga do quadríceps aumentou a base de suporte e reduziu a duração da passada, mas não modificou o posicionamento dos pés em relação ao obstáculo e ao degrau, melhorando o equilíbrio para evitar quedas. Ainda, a mecânica e o controle durante a última passada antes de descer o degrau e a aterrissagemforam dependenteda fadiga nos músculos do tornozelo ou joelho. Foi encontrado que a articulação usada para absorver a energia cinética na descida do degrau após fadiga dos músculos do tornozelo foi dependente da estratégia de descida usada, contato com o calcanhar ou com o metatarso. No entanto, a variabilidade da distancia horizontal pé-obstáculo da perna de abordagem e de suporte foi maior após ambos os protocolos de fadiga, indicando redução no controle do posicionamento do pé. Além disso, os efeitos da fadiga nos músculos do joelho no andar em ambiente regular e irregular de adultos jovens foram independentes do nível de atividade física, mas com efeito do envelhecimento. As modulações espaço-temporal e cinética nas duas tarefas depois da fadiga dos músculos do joelho iniciaram após a idade de 40 anos com estratégia mais arriscada para indivíduos mais velhos (acima de 60 anos). Em conclusão: a) fadiga do quadrícepsafetou negativamente o controle da estabilidade médio-lateral independentemente do tipo de andar, sendo compensado pelas modulações nos parâmetros espaço-temporais e cinéticos, movimento angular, atividade muscular e absorção da energia; b) estratégias musculares compensatórias foram usadas de acordo com o grupo muscular fadigado, recrutando grupos musculares não fadigados para ajustar o padrão de andar e aumentar o equilíbrio. Ainda, a variabilidade da distancia horizontal do pé-degrau dos membros de abordagem e de suporte aumentaram após a fadiga, sugerindo perda de controle; c) o nível de atividade física não interferiu nos efeitos da fadiga dos músculos do joelho do andar em ambiente regular e irregular em adultos jovens. Por outro lado, o envelhecimento teve impacto depois da fadiga dos músculos do joelho. v 9 Palavras-chave: Fadiga muscular; Andar; Obstáculo; Descida de degrau; Envelhecimento; Nível de atividade física; Biomecânica; Controle motor. vi LIST OF CONTENTS CHAPTER 1 - GENERAL INTRODUCTION ...................................................................... 1 1.1. Introduction ......................................................................................................................... 2 1.1.1. Fatigue definition ............................................................................................................. 2 1.1.2. Fatigue prevalence and its effects in daily life ................................................................. 3 1.1.3. Muscle fatigue and aging ................................................................................................. 4 1.1.4. Muscle fatigue and walking .............................................................................................. 4 1.1.5. Aims and outline of this thesis .......................................................................................... 6 CHAPTER 2 - SYSTEMATIC REVIEW OF THE EFFECTS OF FATIGUE ON SPATIOTEMPORAL GAIT PARAMETERS ...................................................................... 8 2.1. Abstract ................................................................................................................................ 9 2.2. Introduction ....................................................................................................................... 10 2.3. Methods ............................................................................................................................. 11 2.3.1. Search strategy ............................................................................................................... 11 2.3.2. Section criteria and quality assessment .......................................................................... 11 2.4. Results ............................................................................................................................... 12 2.4.1. Yield and quality assessment .......................................................................................... 12 2.4.2. Sample characteristics .................................................................................................... 13 2.4.3. Methods to induce muscle fatigue .................................................................................. 15 2.4.4. Spatiotemporal parameters ............................................................................................ 15 2.5. Discussion .......................................................................................................................... 17 CHAPTER 3 - EFFECT OF MUSCLE FATIGUE AND PHYSICAL ACTIVITY LEVEL IN MOTOR CONTROL OF THE GAIT OF YOUNG ADULTS ...................... 21 3.1. Abstract .............................................................................................................................. 22 3.2. Introduction ....................................................................................................................... 23 3.3. Material and methods ........................................................................................................ 24 3.3.1. Participants .................................................................................................................... 24 3.3.2. Experimental design ....................................................................................................... 24 3.3.3. Gait task .......................................................................................................................... 25 3.3.4. Data collection ............................................................................................................... 25 3.3.5. Isometric force measurements ........................................................................................ 25 3.3.6. Fatigue protocol ............................................................................................................ 25 vii 3.3.7. Data analysis ................................................................................................................. 25 3.3.8. Statistical analysis ......................................................................................................... 26 3.4. Results ............................................................................................................................... 27 3.5. Discussion .......................................................................................................................... 31 CHAPTER 4 - INTERACTIONS OF AGE AND KNEE MUSCLE FATIGUE IN WALKING AND OBSTACLE CROSSING ........................................................................ 35 4.1. Abstract .............................................................................................................................. 36 4.2. Introduction ....................................................................................................................... 37 4.3. Material and methods ........................................................................................................ 38 4.3.1. Participants .................................................................................................................... 38 4.3.2. Procedures ...................................................................................................................... 38 4.3.3. Maximum voluntary contraction protocol ...................................................................... 38 4.3.4. Gait trials ........................................................................................................................ 38 4.3.5. Muscle fatigue protocol .................................................................................................. 39 4.3.6. Data analysis .................................................................................................................. 39 4.4. Results ............................................................................................................................... 40 4.4.1. Level gait ........................................................................................................................ 42 4.4.2. Obstacle crossing ........................................................................................................... 42 4.5. Discussion .......................................................................................................................... 46 4.5.1. Level walking..................................................................................................................46 4.5.2. Obstacle crossing ........................................................................................................... 47 4.6. Limitations and conclusion ................................................................................................ 48 CHAPTER 5 - EFFECT OF TRICEPS SURAE AND QUADRICEPS MUSCLE FATIGUE ON THE MECHANICS OF LANDING IN STEPPING DOWN IN ONGOING GAIT ................................................................................................................... 49 5.1. Abstract .............................................................................................................................. 50 5.2. Introduction ....................................................................................................................... 51 5.3. Material and methods ........................................................................................................ 52 5.3.1. Participants .................................................................................................................... 52 5.3.2. Experimental design ....................................................................................................... 52 5.3.3. Fatigue protocols ............................................................................................................ 53 5.3.4. Isometric force measurements ........................................................................................ 54 5.3.5. Stepping task ................................................................................................................... 54 5.3.6. Statistics .......................................................................................................................... 55 5.4. Results ............................................................................................................................... 56 viii 5.5. Discussion .......................................................................................................................... 60 CHAPTER 6 - THE EFFECT OF MUSCLE FATIGUE ON THE LAST STRIDE BEFORE STEPPING DOWN A CURB ............................................................................... 63 6.1. Abstract .............................................................................................................................. 64 6.2. Introduction ....................................................................................................................... 65 6.3. Material and methods ........................................................................................................ 65 6.4. Results............................................................................................................................... 67 6.5. Discussion .......................................................................................................................... 71 CHAPTER 7 - EPILOGUE ................................................................................................... 75 7.1. Effects of quadriceps muscle fatigue on walking in different environments .................... 76 7.2. Ankle muscle fatigue versus knee muscle fatigue: mechanics and control on walking during stepping down ............................................................................................................... 77 7.3. Impact of muscle fatigue in the physical activity level and aging ..................................... 79 7.4. Main considerations and future studies ............................................................................. 80 REFERENCES ....................................................................................................................... 82 ix LIST OF FIGURES Figure 2.1. Flowchart of articles included for review. The number under the text indicates the number of original articles (i.e. not duplicated) at each stage of the search. ...................12� Figure 4.1. Group*fatigue interaction for spatial-temporal variables of level gait. ................44� Figure 4.2. Group*fatigue interaction for spatial-temporal parameters in obstacle crossing………………………………………………………………………………… 46� Figure 5.1. Experimental design. MVC - maximal voluntary contraction. .............................53� Figure 5.2. Use of heel and toe landing as a percentage of all trials before and after fatigue, for (a) ankle muscle fatigue, and (b) knee muscle fatigue. ...............................................56� Figure 6.1. A top view of steps analyzed in the study. Dashed line represents the foot placement. SL – step length; SW – step width; FD – foot distance; L – left leg (trailing foot); R – right leg (leading foot). ....................................................................................66� Figure 6.2. Foot-step distance for trailing (left column) and leading (right column) limbs. The top panels represent the means and standard deviations for each step before and after the fatigue protocols. The lower panels represent the variability (standard deviation) for each step before and after the fatigue protocols. Asterisk (*) indicates significant differences between pre-fatigue and ankle muscle fatigue. Plus (+) indicates significant differences between pre-fatigue and knee muscle fatigue. ..................................................................69� ix x LIST OF TABLES Table 2.1. Methodological quality appraisal results. Y – yes; YL - yes, lacking detail or clarity; N – No; AV – average. A score of one indicated high quality research, with a 0.5 score indicating lack of detail or unclear information and zero indicated lower quality.. 14� Table 2.2. Description articles examined fatigue in walking. YA - young adults; OA - older adults; MVC - maximal voluntary contraction; ST - stride time; SL - stride length; SPL - step length; GS - gait speed; SPW - step width; HCV - heel contact velocity; TA - transitional acceleration. ...................................................................................................16� Table 2.3. Description of articles results per parameter. ↑ - increase after fatigue; ↓ - decrease after fatigue; ~ - similar after fatigue; YA - young adults; OA - older adults; GS - gait speed; SL - stride length; SPL - step length; SPW - step width; ST - stride time; HC - hell contact; HCV - heel contact velocity; ang vel - angular velocity; TA - transitional acceleration; trunk accel - trunk acceleration. ..................................................................18� Table 3.1. Mean and standard deviation of the general characteristics, anthropometric measure, scores on the Multidimensional Fatigue Inventory and Habitual Physical Activity, maximal isometric force before (pre) and after (post) induction to fatigue and endurance time to fatigue for each group. * pre ≠ post; + active group ≠ inactive group. ..........................................................................................................................................28� Table 3.2. Mean and standard deviation of the free and adaptive gait variables. Kinematics variable of approach phase and kinetic variables. BW – body weight. # free gait ≠ adaptive gait. .....................................................................................................................29� Table 3.3. Mean and standard deviation of spatial and temporal parameters according fatigue (independently task and physical activity level) and physical activity level (independently task and fatigue). Kinematic variables of approach phase, crossing obstacle (N) and step after crossing (N+1). LL – leading limb; TL – trailing limb. * pre (before fatigue) ≠ post (after fatigue). ..............................................................................30� Table 3.4. Mean and standard deviation of kinetic parameters according fatigue (independently task and physical activity level) and physical activity level (independently task and fatigue). Kinetic variables of approach phase and crossing obstacle (N). * pre (before fatigue) ≠ post (after fatigue); + active group ≠ inactive group. ..........................................................................................................................................32� x xi Table 4.1. Subject characteristics, endurance time, rating of perceived exertion (RPE) and maximum isometric force for each group. Pre – without muscle fatigue; post – with muscle fatigue. P-values indicate the effects of group. Only for maximal isometric force, p-value indicates interaction group*fatigue...................................................................... 40 Table 4.2. Mean and standard deviations of spatial-temporal and kinetic variables during even gait by group after and before muscle fatigue. For each variable, the first line is before knee muscles fatigue and the second line is after knee muscles fatigue. The last three columns showed the p-values for main effect of group, fatigue and group*fatigue interaction, respectively. ................................................................................................... 43� Table 4.3. Mean and standard deviations of spatial-temporal variables of uneven gait for each group after and before knee muscles fatigue. For each variable, the first line is before knee muscles fatigue and the second line is after knee muscles fatigue. The last three columns showed the p-values for main effect of group, fatigue and group*fatigue interaction, respectively. Foot-obstacle distance - distance between foot and obstacle before crossing the obstacle; obstacle-foot distance - distance between foot and obstacle after crossing the obstacle. ................................................................................................ 45� Table 5.1. Mean values and standard deviations of the endurance times and maximal voluntary isometric contractions (MVIC) before and after fatigue. ................................. 56 Table 5.2. Mean values and standard deviations of parameters characterizing the kinetics during landing (within 200 ms of landing) and spatial-temporal parameters during the step of stepping down before and after ankle muscle fatigue according landing strategy (toe and heel landing). ...................................................................................................... 58� Table 5.3. Mean values and standard deviations of parameters characterizing the kinetics during landing (within 200 ms of landing) and spatial-temporal parameters during the step of stepping down before and after knee muscle fatigue. ........................................... 59 Table 6.1. Mean and standard deviations of spatial-temporal parameters, joint ROM and EMG parameters before (pre-fatigue) and after fatigue (ankle and knee muscle fatigue). The first p-values are comparison between pre-fatigue and ankle muscle fatigue in the Post-hoc test; the second p-values are comparison between pre-fatigue and knee muscle fatigue in the Post-hoc test. ............................................................................................... 70� xii Table 6.2. Variability (standard deviation) of spatial-temporal parameters, joint ROM and EMG parameters before (pre-fatigue) and after fatigue (ankle and knee fatigue). The first p-values are comparison between pre-fatigue and ankle muscle fatigue in the Post-hoc test; the second p-values are comparison between pre-fatigue and knee muscle fatigue in the Post-hoc test. ............................................................................................................... 72 1 Chapter 1 General introduction 2 1.1. Introduction Fatigue is generally considered a safety hazard, and may for example increase the risk of falling (Parijat and Lockhart, 2008a,b). The increasing prevalence of fatigue and its conception as a safety hazard has lead to increased regulation of fatigue by governments (Dawson and McCulloch, 2005). Although fatigue can be considered a negative consequence of physical activity, it also functions as a safety mechanism, as it limits exertion and as such may prevent injury due to overexertion (Ratel et al., 2006; Abbiss and Laursen, 2005;). Fatigue involves a feeling of tiredness, reduced energy and muscle weakness (Kroenke et al., 1988). The latter aspect of fatigue, indicated by a decreased force producing capacity is defined as muscle fatigue, and forms the main interest of this thesis in which the mechanics and motor control of walking with muscle fatigue are studied. The main aim was to understand the mechanics and control adjustments with muscle fatigue during walking in different environments. This might help to identify the impact of fatigue on walking, and contribute to the prevention of falls. In this general introduction, fatigue was defined and then an overview was given of prevalence of fatigue in society to illustrate the importance of studying fatigue in daily activities. Next, the relation between muscle fatigue and aging and subsequently the effects of fatigue on walking were described, indicating the lack of data on fatigue effects on walking in complex environments. Finally, the aims and the outline of this thesis were specified. 1.1.1. Fatigue definition Diverse definitions on fatigue have been formulated, which vary considerably in theirdescription causes, defining attributes, related factors and how the condition might best be alleviated (Trendall, 2000; Ream and Richardson, 1996). The multidimensional characteristic of fatigue complicates a clear definition.Fatigue may be a conceptwhose subjective experience alters rapidly (Hangelin et al., 2007). Normally, fatigue is scaled and defined according to general fatigue, physical fatigue, reduced motivation, reduced activity, and mental fatigue (Smets et al., 1995). However, muscle fatigue can more clearly be defined. Traditionally, muscle fatigue has been defined as the failure to maintain a required or expected force (Edwards, 1981), or the failure to continue working at a given exercise intensity (Booth and Thomason, 1991) or as a loss of muscle performance during repeated or continuous activation (Stackhouse et al., 2001). Closely related to this is the concept ofendurance, whichdescribes the time to failure in 3 maintaining a target muscle force or power output (Kent-Braun, 2009; Hocks et al., 2001). However, as fatigue develops from the onset of activity, a more useful definition of muscle fatigue is given in terms of the capacity to produce muscle force or power (Bigland-Ritchie and Woods, 1984), which can thus be operationalized as a decline in the force generation capacity of muscle over or after a series of repeated contractions or sustained contractions (Kent-Braun, 2009; Gandevia, 2001). Due to thesis context, the definition related to endurance (Kent-Braun, 2009; Hocks et al., 2001) was used for this thesis. 1.1.2. Fatigue prevalence and its effects in daily life Fatigue is recognized as a serious social problem, and an important prerequisite in its prevention is the ability to evaluate fatigue development during daily activities living (Hancock and Desmond, 2000; Cohen et al., 1995). Due to the use of different definitions, reports on the prevalence rate of fatigue in daily activities are inconsistent. The fatigue prevalence is measured according to a general fatigue, which is subjective and causes difficult in the interpretation.Nevertheless, demography studies are indicated that prevalence rates vary from 7 to 42% in the general population (Loge et al., 1998; Pawlikowska et al., 1994; Chalder et al., 1993; Chen, 1986) and depend on gender, age, and physical activity level. There is no specific data on the prevalence of muscle fatigue in society. Muscle fatigue, however, appears to be an important factor in performance of daily activities. For example, many workers are affected by muscle fatigue (Swaen et al., 2003; Tralongo et al., 2003) and studies have shown that between 25% and 33% of falls in the work place occur due to the fatigue (Swaen et al., 2003; Bentley and Haslam, 1998). Muscle fatigue decreases some aspects of motor control and efficiency of performance in daily activities (Ribeiro et al., 2007), which may have functional consequences. For example, increased muscle fatigue may limit the number of stairs that a person can descend or ascend, or cause problems in crossing or circumventing an obstacle, leading to functional limitations and hazards in activities of daily living. Liao et al. (2000) indicated that muscle fatigue influenced functional ability as reflected in walking, cleaning the house, general household chores, getting exercise, and lifting things. In addition, adequate muscle strength in the lower limb muscles has been shown to be required to maintain functional independence in ambulatory activities (Petrella et al., 2005). Therefore, muscle fatigue can contribute to disability, regarding occupational activities and activities of daily living and as such be the cause of a deterioration in quality of life. 4 1.1.3. Muscle fatigue and aging With aging the musculoskeletal and neuromotor systems deteriorate (Kang and Dingwell, 2008; Norris et al., 2007), which might be related to muscle fatigue. Ninety percent of older people show one or more impairments that negatively affect their mobility (Theou et al., 2008). The main impairments are related with dysfunction of muscle (Ross et al., 1997) and proprioception (Shaffer and Harrison, 2007). Importantly age-related alterations include substantial loss of muscle strength and slowed contractile characteristics (Allman and Rice, 2002; Hunter et al., 1998). Despite the high prevalence in the general population, fatigue appears to vary according to the population’s age. In one study 83% of young adults reported moderate or severe fatigue (Amaducci et al., 2010), while in another study more than 50% of adults between 50 and 65 years old reported to be fatigued (Santos-Eggimann et al., 2009) and in another study, 98% of respondents above 70 years old reported fatigue symptoms, with 40% reporting moderate fatigue and 7% severe fatigue (Liao and Ferrell, 2000). However, it is questionable whether these studies can be compared directly, given differences in methods and population characteristics. Overall, age effects on muscle fatigue also remain unclear (Yassierli and Nussbaum, 2007), with several studies showing less fatigue in elderly (Lanza et al., 2004; Tralongo et al., 2003; Watt et al., 2000) and some an increase of fatigue with age (Kent-Braun, 2009; Baudry et al., 2007; McNeil and Rice, 2007; Mens-Verhulst and Bensing, 1998; Lawrie et al., 1997). These inconsistencies may be due to differences in contraction modes, protocol, muscle group or subject characteristics (Kent-Braun, 2009; Katsiaras et al., 2005). Nevertheless, the age of the subjects may be important in fatigue response (McNeil and Rice, 2007). Therefore, age is an important consideration in studies of fatigue and its effects on motor performance (Allman and Rice, 2002). 1.1.4. Muscle fatigue and walking The negotiation of obstacles and uneven surfaces form an important aspect of walking in daily life (Berard and Vallis, 2006). In real life, individuals frequently step up or down level change, and cross or circumvent obstacles in ongoing gait, such as when stepping on or off the sidewalk to cross a street and when crossings a hole or an object on the street or in the home.These tasks require gait adjustment, which may threaten stability. Stability during locomotion is maintained through reactive, predictive, and anticipatory strategies and mainly involves moving the base of support relative to the body mass (Patla, 2003). However, while 5 gait on even surfaces has been extensively studied, negotiation of obstacles and uneven surfaces is comparatively uncharted, especially when other aspects are involved, such as fatigue, aging, and physical activity level. Obstacle crossing causes adjustments during walking, in which the individual modulates the foot-obstacle distance and toe-clearance to safely cross the obstacle (Silva et al., 2011; Gobbi et al., 2009; Siu et al., 2008; Di Fabio et al., 2004;Hedel et al., 2002). In addition, while crossing over an obstacle, gait velocity is reduced by reducing step length and cadence (Lowrey et al., 2007). With respect to uneven surfaces, while stepping down a height difference, step size is adjusted to allow the last step on the high level to land close to the height difference (Begg and Sparrow, 2000; Crosbie and Ko, 2000), and the forward and linear angular momentum gained during stepping down are reduced by making a larger step with the leading leg (Dieën et al., 2008). Failure to do so can cause a loss of balance (Dieën et al., 2008). Various factors can affect walking in a more complex environment. For example; a) with aging, cadence and stride duration are increased and walking velocity and stride length are decreased (Owings and Grabiner, 2004; Shkuratova et al., 2004); b) low physical activity level is associated with poor balance and propulsion (Petrella et al., 2005; Sadeghi et al., 2004; Merletti et al., 2002). On the other hand, motor control literature has emphasized the ability to adapt motor behavior to destabilizing conditions to reduce error probability (Diëen and Pijnappels, 2009), such as when fatigue destabilizes motor performance and decreases muscle strength (Gates and Dingwell, 2008; Selen et al., 2007). Adequate muscle strength in lower limb muscles is required for safely crossing an obstacle and stepping down a curb (Petrella el al., 2005). Muscle fatigue can impair motor control by increasing muscle co- contraction and limiting fast corrective movements (Izawa et al., 2008; Franklin et al., 2007; Dieën et al., 2003), and by adversely affecting proprioception, movement coordination and muscle reaction times (Lin et al., 2009; Parijat and Lockhart, 2008a), which are important components of balance control (Parijat and Lockhart, 2008a,b; Helbostad et al., 2007; Lord et al., 1993).A new segmental organization in the presence of muscle fatigue is required to maintain motor performance, as observed by changes in time and spatial gait parameters (Murdock and Hubley-kozey, 2011; Olson, 2010; Granacher et al., 2010; Lin et al., 2008; Parijat and Lockhart, 2008a,b; Helbostad et al., 2007; Kavanagh et al., 2006; Yoshino et al., 2004). Thus, a relationship between muscle fatigue in the lower extremities and deficits in the control of gait is likely. However, to our knowledge, there is no study available that investigated the impact of muscle fatigue on walking in complex environments, such as in obstacle crossing and 6 stepping down a curb. The understanding of muscle fatigue effects could help to avoid falls, slip, trips and injuries during walking in complex environments. Furthermore, fatigue may be a useful model to study the effects of disease as it impairs muscle torque-generating capacity, yet does not have confounding factors like pain or swelling (Murdock and Hubley-Kozey, 2011). 1.1.5. Aims and outline of this thesis The aim of the study is to analyze the effects of muscle fatigue on mechanics and motor control of walking in different environments. A series of walking experiments addressed muscle fatigue impact have been conducted, in order to obtain the required information. The chapters arising from these studies address the following topics: the effects of muscle fatigue on walking, muscle fatigue impact on walking in different environments, age-related changes in control of gait with muscle fatigue, and effects of fatigue in different muscular group on mechanics and control of gait during stepping down. First, we analyzed the effects of fatigue on gait by means of a systematic review (Chapter 2). In this chapter, we tried to determine the effects of fatigue on gait on even ground and the gaps in our knowledge in this context. The specific question addressed was: What are the effects of fatigue on the spatiotemporal characteristics of gait? Second, we investigated whether the fatigue impact is similar in walking in different environments. For this, we analyzed the effect of muscle fatigue in young adults on the kinematic and kinetic parameters of even walking and obstacle crossing (Chapter 3). The complexity of obstacle crossing could change the strategy and the stability of walking with muscle fatigue. In the Chapter 4, a similar study was performed but age-related effects were included. We expected that the effects of muscle fatigue on gait would be increased with aging. Thirdly, we examined the changes in the mechanics and control of gait in negotiating level changes when quadriceps or triceps surae muscles were fatigued. In Chapter 5, the aim was to evaluate the effects of muscle fatigue on mechanics and stability of stepping down in ongoing gait. The participants performed a fatigue protocol on two different days (one day for the quadriceps muscles and another day for the triceps surae muscles). The hypotheses were: a) a shift of negative work from the fatigued muscles to non-fatigued muscles; b) increased negative work at landing and a conservative gait pattern with fatigue. Chapter 6 reports the effects of quadriceps and triceps surae muscle fatigue during the approach phase before 7 stepping down. We specifically address the variability of foot placement and other kinematic parameters as well as electromyography parameters. Finally, in Chapter 7, the main findings and conclusions of this thesis are summarized and a number of recommendations for further research are provided. 8 Chapter 2 Systematic review of the effects of fatigue on spatiotemporal gait parameters Accepted to Journal of Back and Musculoskeletal Rehabilitation 9 2.1. Abstract This systematic review aimed to assess changes in spatiotemporal gait parameters due to fatigue. A search was carried out in literature published from 1950 to December 2010 and retrieved 771 articles using terms referring to walking and fatigue in the title, abstract or keywords. Two researchers assessed the selection and quality of each article independently. Seven studies were selected for this systematic review, two of which reported on the same data set. Several biomechanical parameters were reported to change with fatigue, but the few variables studied in multiple studies, gait speed and stride or step length and stride time were affected only in single studies. Fatigue appears to modulate spatiotemporal gait parameters, but the effects of fatigue appear to be dependent on the muscles that are fatigued and age appears to be a moderator of the effects of fatigue on gait. 10 2.2. Introduction Fatigue is used to describe a number of phenomena with a variety of causes (Ergenton et al., 2009), but may be more strictly defined as any exercise-induced reduction in the ability of a muscle to generate force or power (Edwards, 1981), or failure tocontinue working at a given exercise intensity (Booth and Thomason, 1991). Fatigue development is mediatedbya range of individual factors such as the presence of pathology, age (older adults fatigue faster than young adults), physical activity level (inactive individuals fatigue faster than active individuals), and the type of activity performed.Fatigue not only affects elderly and diseased populations, as 5-56% of employees in 15 European countries reported fatigue at work (Benavides et al., 2000)and one-third of the US workforce experienced fatigue in the workplace (Swaen et al., 2003). Fatigue is considered as a safety mechanism to prevent injury (Ratel et al., 2006; Abbiss and Laursen, 2005), but it may have negative effects on activities of daily living (ADL) (Liao and Ferrell, 2000). For example, walking distance, cleaning the house, general household chores and getting exercise are limited by fatigue (Tralongo et al., 2003). Therefore, fatigue can contribute to disability, regarding occupational activities and ADL and as such be the cause of a deterioration in independence and quality of life. Furthermore fatigue adversely affects proprioception, movement coordination and reaction times (Lin et al., 2009), and consequently has negative effects on motor control (Ribeiro et al., 2007). For example, fatigue may compromise balance control and predispose to falls (Helbostad et al., 2010; Lin et al., 2009; Parijat and Lockhart, 2008a,b; Helbostad et al., 2007). In an investigation of slip and fall accidents among postal delivery workers in the UK (Bentley and Haslam, 1998), fatigue was found to be a precursor of 25% of all fall incidents. The literature provides some evidence of fatigue-related changes of the biomechanical characteristics of gait, indicating that a new segmental organization occurs in the presence of muscle fatigue, as observed by changes of spatiotemporal gait parameters (Murdock and Hubley-Kozey, 2012; Olson, 2010; Granacher et al., 2010; Lin et al., 2009; Parijat and Lockhart, 2008a,b; Helbostad et al., 2007; Kavanagh et al., 2006; Yoshino et al., 2004). However, a comprehensive overview of which gait parameters and how these parameters are changed by fatigue is lacking. Therefore, a systematic review was performed with the aim to assess changes of spatiotemporal gait parameters due to fatigue. An understanding of fatigue effects on walking could help to avoid falls, slip, trips and injuries (Murdock and Hubley- Kozey, 2012), and as such improve quality of life. 11 2.3. Methods 2.3.1. Search strategy The initial search strategy was performed to identify all articles on the effect of fatigue on spatiotemporal gait parameters. An electronic search was conducted in 6 databases: Cochrane Library, Embase, Medline – ISI, PsycInfo, PubMed, and Web of Science – ISI. We searched articles from 1950 to December 2010. Targeted searching of frequently cited journals, authors and article reference lists ensured that all relevant articles were located. To be deemed relevant for review, an article had to contain terms referring to walking and fatigue in the title, abstract or keywords. The word gait was used together walking due to the similarity in the terminology. Key terms within the search strategy were also matched using medical subject headings (MeSH) in databases such as Medline. Articles on animal studies, robotics, children and reviews, methodological or descriptive papers were excluded using another set of key terms. As an example, the following search strategy was used in the PubMed: “gait OR walking AND fatigue” searched in the title/abstract, with following limits: language – English; type of article – clinical trial, randomized controlled trial and journal article; species: humans. 2.3.2. Section criteria and quality assessment The initial yield was obtained by combining all original articles from electronic databases and targeted searches. Articles not relating to walking were excluded during an initial screening of titles and abstracts. The remaining abstracts were checked against the inclusion/exclusion criteria. The full text was examined if the abstract contained insufficient information to decide on inclusion. Two reviewers screened all articles for inclusion. A set of guidelines and examples for completing article reviews was provided to both reviewers to improve inter-reviewer reliability. The two researchers independently assessed the selection and quality of each article. Only English language articles were considered for analysis. Studies that investigated effects of fatigue on gait in health young, middle-aged and older adults, but not pathological individuals were initially selected. If a study investigated both walking freely on flat ground and another form of locomotion or walking with concurrent task, only details pertaining to effects of fatigue in the walking freely on flat ground were considered. Articles were included in the systematic review if they investigated the effects of fatigue in walking freely on flat ground on spatiotemporal parameters. As differences in terminology and writing style exist 12 between researchers, a list of synonyms for spatiotemporal (step or stride length and width, stride time, speed, velocity, acceleration, spatiotemporal and spatial-temporal) was used for each key term to identify all relevant articles. Studies on treadmill walking were excluded because gait adaptations on a treadmill may be different from those in over ground walking. The quality of a study was defined as its capacity to avoid potential bias and to generate results that can be generalized. We used a quality appraisal tool developed by Galna et al. (2009), which is specific for this type of systematic review. A scoring system was used to quantify the quality of each study and to assess its methodological strengths and weaknesses. Each question on the quality appraisal tool was scored with a maximum of one, indicating high quality research, with a 0.5 score indicating lack of detail or unclear information and a zero score indicating low quality. Study quality was used to weigh the evidence in case of conflicting outcomes. 2.4. Results 2.4.1. Yield and Quality Assessment The search in the databases revealed 771 articles (Figure 2.1). Following abstract review, 81 articles were related to effect of fatigue in gait on spatiotemporal parameters. The final yield included seven articles that analyzed effects of fatigue on spatiotemporal parameters of gait. Two papers reported data collected in the same experiment (Parijat and Lockhart, 2008a,b), leaving six papers for review. Figure 2.1. Flowchart of articles included for review. The number under the text indicates the number of original articles (i.e. not duplicated) at each stage of the search. 13 Table 2.1 summarizes the quality assessment for these papers. Overall, quality was satisfactory, the articles stated the aims with sufficient clarity, gave an appropriate description of the participants, detailed the key outcomes clearly, employed a suitable methodology, discussed the results appropriately and indicated implications. One important shortcoming in the statistical analysis was noted for the study by Yoshino et al. (2004). In this study, subjects were sub-grouped based on the kinematic changes that occurred due to fatigue (duration of stride time). This makes it impossible to judge whether changes in spatiotemporal parameters were significant at the group level. Nevertheless the results of the largest subgroup (8 vs 4 subjects) were included in the review. Most investigations controlled for age and gender, but typically did not control for height, limb asymmetries and strength differences between groups. Details provided were adequate to replicate the studies, although methods for inclusion/exclusion criteria were often not reported. No study completely described the recruitment and sampling methods. The reliability of key outcome measures and the internal validity of the key outcome measures were reported in only one study. 2.4.2. Sample Characteristics Both male and female participants were recruited in the studies analyzed (Table 2.2), except for three studies in which participants of one sex were recruited: one study included only females (Olson, 2010) and two studies included only males (Kavanagh et al., 2006; Yoshino et al., 2004). Four studies (Parijat and Lockhart, 2008b; Kavanagh et al., 2006; Yoshino et al., 2004; Olson et al., 2010) analyzed the influence of muscle fatigue in young adults, while one paper (Helbostad et al., 2007) evaluated the effect of fatigue on gait in elderly. A single study (Granacher et al., 2010) compared the effects of fatigue on gait between age groups (young vs older adults). In the seven papers, the mean age of the young adults ranged from 20 to 34 years and of the older adults it ranged from 71 to 81 years. 1 T ab le 2 .1 .M et ho do lo gi ca l q ua lit y ap pr ai sa l r es ul ts . Y – y es ; Y L - y es , l ac ki ng d et ai l o r c la rit y; N – N o; A V – a ve ra ge . A s co re o f o ne in di ca te d hi gh q ua lit y re se ar ch , w ith a 0 .5 sc or e in di ca tin g la ck o f d et ai l o r u nc le ar in fo rm at io n an d ze ro in di ca te d lo w er q ua lit y. Q ue st io n Sc or in g cr ite ri a Y os hi no e t al . ( 20 04 ) K av an ag h et al . ( 20 06 ) H el bo st ad e t al . ( 20 07 ) Pa ri ja t e t a l. (2 00 8a ,b ) G ra na ch er e t al . ( 20 10 ) O ls on (2 01 0) 1. R es ea rc h ai m s o r q ue st io ns st at ed c le ar ly 1 – Y ; 0 .5 – Y L; 0 - N 1 1 1 1 1 1 2. P ar tic ip an ts d et ai le d N um be r 1 1 1 1 1 1 A ge 1 1 1 1 1 1 Se x 1 1 1 1 1 1 H ei gh t 0 1 0 1 1 1 Su b To ta l 0. 75 1 0. 75 1 1 1 3. R ec ru itm en t a nd sa m pl in g m et ho ds d es cr ib ed 1 – Y ; 0 .5 – Y L; 0 - N , 0 0. 5 0. 5 0 0. 5 0 4. In cl us io n an d ex cl us io n cr ite ria d et ai le d 1 – Y ; 0 .5 – Y L; 0 - N 0 0. 5 1 0. 5 1 0. 5 5. C on tro lle d co va ria te s H ei gh t 0 0 0 0 0 0 W al ki ng S pe ed 1 0 1 0 1 1 A ge 1 1 1 1 1 1 G en de r 1 1 0 1 1 1 Li m b A sy m m et rie s 0 0 0 0 1 0 St re ng th 0 1 0 1 1 0 Su b To ta l 0. 5 0. 5 0. 33 0. 5 0. 83 0. 5 6. K ey o ut co m e va ria bl es c le ar ly d es cr ib ed 1 – Y ; 0 .5 – Y L; 0 - N 1 1 1 1 1 1 7. A de qu at e m et ho do lo gy a bl e to re pe at st ud y Pa rti ci pa nt sa m pl in g 0 1 1 1 1 1 Eq ui pm en t 1 1 1 1 1 1 Pr oc ed ur e 1 1 1 1 1 1 D at a pr oc es si ng 1 1 1 1 1 1 St at is tic al a na ly si s 1 1 1 1 1 1 Su b to ta l 0. 8 1 1 1 1 1 8. M et ho do lo gy a bl e to a ns w er re se ar ch q ue st io n Pa rti ci pa nt sa m pl in g 1 1 1 1 1 1 Eq ui pm en t 1 1 1 1 1 1 Pr oc ed ur e 1 1 1 1 1 1 D at a pr oc es si ng 1 1 1 1 1 1 St at is tic al a na ly si s 0 1 1 1 1 1 Su b to ta l 1 1 1 1 1 1 9. R el ia bi lit y of th e m et ho do lo gy st at ed 1 – Y ; 0 – N 0 0 0 0 0 0 10 . I nt er na l v al id ity o f t he m et ho do lo gy st at ed 1 – Y ; 0 – N 0 0 0 0 0 0 11 R es ea rc h qu es tio ns a ns w er ed a de qu at el y in th e di sc us si on 1 – Y ; 0 – N 1 1 1 1 1 1 12 . K ey fi nd in gs su pp or te d by th e re su lts 1 – Y ; 0 – N 1 1 1 1 1 1 13 . K ey fi nd in gs in te rp re te d in a lo gi ca l m an ne r w hi ch is su pp or te d by re fe re nc es 1 – Y ; 0 – N 1 1 1 1 1 1 14 . C lin ic al im pl ic at io ns st at ed 1 – Y ; 0 .5 – Y L; 0 - N 0. 5 1 1 1 1 1 14 15 2.4.3. Methods to Induce Muscle Fatigue Protocols used to induce fatigue differed between the studies analyzed including isometric contractions at different percentages of maximal voluntary contraction (Olson, 2010; Kavanagh et al., 2006), isokinetic exercise (Granacher et al., 2010; Parijat and Lockhart, 2008a,b), repeated sit-to-stand transfers (Helbostad et al., 2007) and walking itself (Yoshino et al., 2004). When isometric and isokinetic contraction were used, the loads ranged from 50% to 70% of the maximum. Regarding the time to execute the fatigue protocol, studies used a fixed time period (Kavanagh et al., 2006; Yoshino et al., 2004), or the time that participant could maintain performance at a given contraction level (Granacher et al., 2010; Olson, 2010; Parijat and Lockhart, 2008a,b), or the time until the participant felt too exhausted to do more repetitions (Helbostad et al., 2007). Moreover, different muscles were fatigued. In three studies the knee extensor muscles were fatigued (Granacher et al., 2010; Parijat and Lockhart, 2008a,b; Helbostad et al., 2007), in two studies the trunk muscles [19,20], and in one study the lower limb muscles (Yoshino et al., 2004). Fatigue as defined by a decrease in force producing capacity of the muscles exercised was confirmed to be present at the end of or after the fatigue protocol in all studies but two (Helbostad et al., 2007; Yoshino et al., 2004). The latter studies did report subjective indications of fatigue and Yoshino et al. (2004) did show indications of muscle fatigue in the EMG of the tibialis anterior muscle in the largest sub-group of subjects in their study. 2.4.4. Spatiotemporal Parameters The spatiotemporal parameters analyzed in the included studies were gait speed, stride and step length, stride time, step width, cadence, trunk accelerations, transitional acceleration and heel contact velocity. In addition, some studies addressed the variability of selected spatial and/or temporal parameters, i.e. of stride time, stride length, step width and trunk accelerations. The results are summarized per study in Table 2.2 and per parameter studied in Table 2.3. 16 T ab le 2 .2 .D es cr ip tio n ar tic le s ex am in ed fa tig ue in w al ki ng . Y A - yo un g ad ul ts ; O A - ol de r a du lts ; M V C - m ax im al v ol un ta ry c on tra ct io n; S T - st rid e tim e; S L - s tri de le ng th ; S PL - st ep le ng th ; G S - g ai t s pe ed ; S PW - st ep w id th ; H C V - he el c on ta ct v el oc ity ; T A - tra ns iti on al a cc el er at io n. A U T H O R S O B JE C T IV E S G R O U P FA T IG U E P R O T O C O L G A IT P A R A M E T E R S FA T IG U E E FF E C T S* Y os hi no e t al . ( 20 04 ) to e xa m in e w he th er g ai t pa tte rn s a nd p hy si ol og ic al rh yt hm s a re a ff ec te d by fa tig ue 12 m al es (1 9- 26 yr s) : G ro up A (lo ng g ai t c yc le ti m e in th e 2° ha lf of p ro to co l) an d G ro up B (s ho rt ga it cy cl e tim e) to w al k 3h c on tin uo us ly a t pr ef er re d pa ce o n gr ou nd le ve l ST , v ar ia bi lit y of S T, tr un k ac ce le ra tio n Y ES ** K av an ag h et al . ( 20 06 ) to e xa m in e ho w fa tig ue af fe ct s t he a bi lit y to m ai nt ai n he ad st ab ili ty du rin g w al ki ng 8 m al es (2 3± 4y rs ) is om et ric c on tra ct io n of lu m ba r a nd c er vi ca l e re ct or sp in al m us cl es : 6 0% M V C (3 0 s c on tra ct io n, 3 0 s r es t) G S, S T, S PL , c ad en ce N O H el bo st ad e t al . ( 20 07 ) to in ve st ig at e th e ef fe ct o f fa tig ue o n tru nk a nd fo ot le ve l g ai t c ha ra ct er is tic s 17 fe m al es a nd 1 0 m al es (f at ig ue g ro up : 7 8. 2± 5y rs ; co nt ro l g ro up : 8 0. 4± 4. 9y rs ) si t-t o- st an d re pe at ed ly fr om a c ha ir at a fa st sp ee d un til fe lt to o ex ha us te d tru nk a cc el er at io n am pl itu de s a nd va ria bi lit y, S PW , v ar ia bi lit y of SP L SP L, G S, v ar ia bi lit y of S PW Y ES N O Pa rij at e t a l. (2 00 8a ,b ) to in ve st ig at e th e ef fe ct s o f lo w er m us cl e fa tig ue o n ga it ch ar ac te ris tic s 6 fe m al es a nd 1 0 m al es (2 4. 6± 3. 5y rs ) is ok in et ic k ne e ex te ns io n at 7 0% M V C u nt il fo rc e dr op s b el ow 6 0% M V C H C V , T A , G S Y ES N O G ra na ch er et a l. (2 01 0) to e xa m in e th e ef fe ct s o f fa tig ue o n ga it un de r s in gl e an d du al -ta sk c on di tio ns 16 fe m al es a nd 1 6 m al es (Y A : 24 .3 ±1 .4 yr s; O A : 7 1. 9± 5. 5y rs ) m ax . i so ki ne tic k ne e ex te ns io n un til fo rc e dr op s be lo w 5 0% M V C Y A : G S, S L O A : G S, S L; Y A a nd O A : S L va ria bi lit y Y ES N O O ls on (2 01 0) to st ud y ch an ge s i n m us cl e ac tiv at io n an d ga it pa ra m et er s w ith fa tig ue 14 fe m al es (2 7. 5± 12 yr s) is om et ric tr un k ex te ns io n at 5 0% o r 7 0% M V C u nt il fo rc e dr op s b el ow 2 0% M V C G S, S T, S L N O * W e in di ca te d on ly st at is tic s e ff ec ts o f f at ig ue fo r f re e ga it. ** In la rg es t s ub -g ro up d ef in ed p os t-h oc b as ed o n in cr ea se in a ve ra ge st rid e tim e. 16 17 2.5. Discussion The following question was addressed in this systematic review: What are the effects of fatigue on the spatiotemporal gait parameters? The literature retrieved was limited in numbers and used widely different protocols to induce fatigue and a range of different dependent variables. Strikingly the most commonly studied variables, gait speed, step or stride length and stride time did not appear to be affected in a majority of studies. Nevertheless, several other gait parameters appear to change due to fatigue, although many were reported in only one or two studies. The effects of muscle fatigue on the spatiotemporal gait parameters appear dependent on the muscles that were fatigued, with changes being more evident when leg muscles were fatigued than when postural (trunk) muscles were fatigued. However, the studies addressing trunk muscle fatigue did not report variables related to trunk movement (e.g. medial-lateral trunk acceleration or angular displacement). Thus, when trunk muscles are fatigued, individuals appear not to modulate lower limb gait kinematics. The knee extensor muscles, which obviously have a more specific role in gait, were fatigued in most of the studies, and although lower limb kinematics appear to be affected the diversity of dependent variables studied precludes definitive conclusions. As for exercise type, the diversity of fatigue protocols used does not allow definitive conclusions. Although isometric protocols may offer a safe, selective and standardized way of fatigue muscles (Ratel et al., 2006), the strategy of neuromuscular recruitment varies according to the task (isometric or isotonic task) (Olson, 2010) and hence results may be influenced by the task used(Ergenton et al., 2009). Therefore, inducing fatigue under dynamic conditions may be more relevant to physical performance during daily living activities (McNeil and Rice, 2007). Induction of fatigue through a functional task like walking or repeated sit-to-stand transfers as used in some of the studies likely has the advantage that results are more representative for daily life conditions. In addition to the type of exercise, the duration of the fatigue protocol may affect the results, specifically because the fatigue effects are measured over a period of walking after the protocol during which recovery may occur. Recovery after short, high-intensity exercise may be relatively fast (Lattier et al., 2004). To reflect daily activity,it has been recommended that the duration of the exercise should be controlled rather than the task intensity or workload(Ergenton et al., 2009). 59 T ab le 2 .3 . D es cr ip tio n of a rti cl es re su lts p er p ar am et er . ↑ - in cr ea se a fte r f at ig ue ; ↓ - de cr ea se a fte r f at ig ue ; ~ - si m ila r a fte r f at ig ue ; Y A - yo un g ad ul ts ; O A - ol de r a du lts ; G S - g ai t s pe ed ; S L - s tri de le ng th ; S PL - st ep le ng th ; S PW - st ep w id th ; S T - s tri de ti m e; H C - he ll co nt ac t; H C V - he el c on ta ct v el oc ity ; a ng v el - an gu la r v el oc ity ; T A - tra ns iti on al a cc el er at io n; tr un k ac ce l - tr un k ac ce le ra tio n. M EA N V A LU ES V A R IA B IL IT Y G ai t sp ee d St rid e/ St ep le ng th St ep w id th C ad en ce St rid e tim e H ee l co nt ac t ve lo ci ty Tr an si tio na l ac ce le ra tio n Tr un k ac ce le ra tio n St rid e/ St ep le ng th St ep w id th St rid e tim e Tr un k ac ce le ra tio n Y os hi no e t a l. (2 00 4) * ↑ ↓ ↑ K av an ag h et a l. (2 00 6) ~ ~ ~ ~ H el bo st ad e t a l. (2 00 7) ~ ~ ↑ ↑* * ↑ ~ ↑ Pa rij at e t a l. (2 00 8a ,b ) ~ ↑ ↓ G ra na ch er e t a l. – Y A (2 01 0) ↓ ↓ ~ G ra na ch er e t a l. – O A (2 01 0) ~ ~ ~ O ls on (2 01 0) ~ ~ ~ * In la rg es t s ub -g ro up d ef in ed p os t-h oc b as ed o n in cr ea se in a ve ra ge st rid e tim e ** In fr ai l e ld er ly o nl y 18 19 Only one study directly compared young and old adults, hence no definitive conclusion on the moderating effect of age can be made. The results of this study (Granacher et al., 2010), with reductions in gait speed and stride length in young adults only, suggest that young adults use a more conservative strategy (Gobbi et al., 2011; Patla, 2003) with muscle fatigue. Also other studies with young adult participants only showed indications of a more conservative strategy possibly to prevent slips, although heel contact velocity increased with fatigue, which would increase slip risk (Lockhart et al., 2005). Overall, young adults seem to modulate gait performance to increase safety. In older adults the gait pattern appears less robust with fatigue, as indicated by increased trunk accelerations and increased variability of stride length and trunk acceleration, possibly as direct effects of fatigue and concomitant loss of control (Mbourou et al., 2003; Brach et al., 2001). As possible adaptations, older adults did show an increase of step width (Helbostad et al., 2007; Helbostad and Moe-Nilssen, 2003), which would increase medio-lateral stability of gait (Hof et al., 2007). Remarkably, no evidence was found for reductions in gait speed and stride length in older adults. An increase in gait speed may decrease the mediolateral displacement of the center of mass, further contributing to medio-lateral balance control (Staszkiewicz et al., 2010; Lee and Chou, 2006; Orendurff et al., 2004). There may be a U-shaped relation between fall risk and gait speed(Helbostad and Moe-Nilssen, 2003). Possibly young adults normally walk above the speed at which their fall risk is minimal, making a decrease in speed useful for them to decrease their risk in case of fatigue. A similar decrease might not be effective in older adults who already prefer lower walking speeds than young adults (Lockhart et al., 2005). With fatigue spatiotemporal gait parameters appear to be modulated. However, the adjustments appear to be dependent of the muscles that are fatigued, the type and duration of exercise and on the subjects’ age. Fatigue coincides with a decrease in muscle strength (Ergenton et al., 2009; Petrella et al., 2005), reduced proprioceptive acuity, and delayed neuromuscular responses (Taimela et al., 1999). These changes are likely to increase fall risk during gait. Some of the changes in biomechanical gait parameters (increased heel contact velocity, increased trunk acceleration and increased variability of stride length) appear to reflect this increased risk of falling. However, simultaneously others changes (increased step width, reduced gait speed and stride length) may reflect adaptations to counteract the increase of the risk of falling. Several limitations from this review are evident. Despite of importance the fatigue in the daily activities and gait, few studies have addressed this issue. More studies are required to understand the effects of fatigue on gait with careful consideration of subjects’ age and the 20 muscle that are fatigued as well as the type of exercise used to do so. From the literature reviewed, we conclude that: a) fatigue appears to modulate the spatiotemporal parameters of gait b) the effects of fatigue on the spatiotemporal gait parameters appear dependent on the muscles that are fatigued; c) age appears to be a moderator of the effects of fatigue on gait. 21 Chapter 3 Effect of muscle fatigue and physical activity level in motor control of the gait of young adults Submitted to Gait and Posture 22 3.1. Abstract The aim of this study was to analyze the effect of muscle fatigue in active and inactive young adults on the kinematic and kinetic parameters of normal gait and obstacle crossing. Twenty male subjects were divided into active (10) and inactive (10), based on self-reported physical activity. Participants performed three trials of two tasks (normal gait and obstacle crossing) before and after a fatigue protocol, consisting of repeated sit-to-stand transfers until the instructed pace could no longer be maintained. MANOVAs were used to compare dependent variables with the following factors: physical activity level, fatigue and task. The endurance time in the fatigue protocol was lower for the inactive group. Changes of gait parameters with fatigue, among which increased step width and increased stride speed were the most consistent, were independent of task and physical activity level. These findings indicate that the kinematic and kinetic parameters of gait are affected by muscle fatigue irrespective of the physical activity level of the subjects and type of gait. Inactive individuals used a slightly different strategy than active individuals when crossing an obstacle, independently of muscle fatigue. 23 3.2. Introduction Fatigue affected the performance of daily activities, such as walking. To maintain motor performance in the presence of fatigue, adjustments in temporal and spatial parameters of gait are required (Parijat and Lockhart, 2008a,b; Helbostad et al., 2007). Fatigue effects are task-dependent (Brujin et al., 2009; Enoka and Duchateau, 2008) and may thus be different for gait in environments of different complexity. While fatigue effects on gait characteristics have been studied to some extent in an unobstructed environment allowing free gait, characteristics of adaptive gait for example to cross or circumvent obstacles, as is commonly required in daily locomotion (Vitório et al., 2010), has to our knowledge not been studied previously. Gait characteristics appear to be influenced by physical activity levels, with inactive individuals showing differences from active individuals in free gait reflective of a poor neuromuscular condition affecting both balance control and propulsion (Gotshalk et al., 2008; Katsiaras et al., 2005). In adaptive gait, inactive individuals showed a lower walking speed and increased foot-obstacle horizontal distance of the leading limb compared to active individuals (Niang and McFadyen, 2005). Physical activity levels also mediate fatigue development (Katsiaras et al., 2005), with inactive individuals being more fatigable than active individuals (Viner et al., 2008), and may alter fatigue effects on motor performance. The aim of this study, therefore, was to analyze the effects of muscle fatigue in active and inactive young adults on the kinematic and kinetic parameters of free and adaptive gait. We expected that the motor control of free and adaptive gait would be dependent on the physical activity level before and after fatigue induction and hypothesized interaction effects between physical activity level and fatigue. Furthermore, we expected that muscular fatigue affect free and adaptive gait differently. We analyzed spatial-temporal gait characteristics, which have been related to fall risk or have been shown adapted to decrease fall risk (e.g. gait speed, step duration, step width). In addition, we looked at the spatial relations between the feet and the obstacle, which determine the probability of tripping over or stepping on the obstacle. Finally, we analyzed vertical ground reaction forces to characterize weight acceptance and horizontal forces to provide insight into how speed is modulated. 24 3.3. Material and Methods 3.3.1. Participants Thirty young male adults participated of this study. The exclusion criteria of the study were factors that could interfere with gait and other experimental procedures, such as medication use, presence of osteomyoarticular, neuromuscular or cardio-respiratory diseases and balance and vision disorders. Ten recruited subjects did not fit the criteria of the study. So, twenty individuals were included in the study sample. Theywere distributed into active and inactive (Table 3.1). The study was approved by the local Ethics Committee (2055/2008). The active group was composed of individuals who performed physical activity for more than three months for at least three times a week and at least one hour per day and the inactive group was composed of individuals who had not performed regular physical activity in at least the last three months (Greaves et al., 2011; Florindo et al., 2009). In addition, participants filled out the Questionnaire of Habitual Physical Activity (Baecke et al., 1982). In this questionnaire the responses are scored on a five-point scale and result in three different indices reflecting physical activity during work, leisure time excluding sport and sport activities. The summation of the three indices was defined as the overall physical activity index. The values for the active group were ≥ 9 and the inactive group scored ≤7 (Cocker et al., 2009). 3.3.2. Experimental design Participants were instructed not to perform any strenuous physical activity 48h before evaluation. The experiment was divided into two days. On the first day, participants filled out a questionnaire on medical history, the Questionnaire of Habitual Physical Activity and the Multidimensional Fatigue Inventory (Smets et al., 1995). The latter was used to determine the presence of fatigue prior to study, and no fatigue was found for both groups (Table 3.1). In addition, the anthropometric measurements were performed. At the beginning of the second day, there was a warm-up period of 5min, with walking, stretching and movements in the Leg Press. After that, participants performed the trials of free and adaptive gait following the maximum voluntary isometric contractions. Immediately after the he maximum voluntary isometric contractions, the fatigue protocol was performed. Subsequently, the gait tests and the maximal voluntary contractions were performed once again. 25 3.3.3. Gait task Three trials for each experimental condition, free and adaptive gait, with the order randomly defined were performed before and after the fatigue protocol. The starting point of each gait trial was adjusted to ensure that the obstacle was crossed with the right leg and that at least two strides were completed prior to obstacle crossing. The instruction given to the participant was to walk over an 8m pathway, at self-selected speed. For the adaptive gait trials, the participant was instructed to avoid contact with the obstacle (15 cm high, 80 cm wide and 2 cm thick), which was positioned between two force platforms. For free gait we analyzed the stride (period between two consecutives heel contacts of the left limb) in the middle of the pathway, which was compared to the stride preceding the obstacle crossing for adaptive gait (approach phase). For adaptive gait, we additionally analyzed the crossing step (from heel contact of the left limb in front of the obstacle to heel contact of right limb behind the obstacle) and the step (from heel contact of the right limb behind the obstacle to heel contact of left limb behind the obstacle) after crossing the obstacle (N+1). 3.3.4. Data collection Ground reaction forces were measured using two force plates (AccuGait, Advanced Mechanical Technologies) at a sample rate of 200 samples/s, positioned across the central area of the pathway (20 cm away from each other). Acquisition of kinematic gait parameters was accomplished with a three-dimensional optoelectronic system (OPTOTRAK Certus), positioned in the sagittal right plane, using a sample rate of 100 samples/s. Four infrared emitters were placed over the following anatomical points: lateral face of calcaneus and head of the fifth metatarsus of the right limb, and medial face of calcaneus and head of the first metatarsus of the left limb. To determine the heel contact and toe-off of the limbs during gait, only the markers on the calcaneus and toe were used (O’Çonnor et al., 2007). The data acquisition systems were electronically synchronized. 3.3.5. Isometric force measurements After the free and adaptive gait trials, maximum voluntary isometric contractions were performed in a Leg Press device (Gotshalk et al., 2008). A load cell with precision of 0.98N was used in combination with a signal amplifier (EMG System do Brasil Ltda.). The participant performed the test with both legs, with the instruction to produce maximum force as fast as possible. Total contraction duration was 5 s. The participants were seated in a backward inclined chair, with the hip joint at 90° (180° is full extension) and knee joint at 26 110° (180° is full extension). Participants performed two attempts before and after the fatigue protocol, with 2 min rest between attempts. The means of the two attempts before and after muscle fatigue were calculated for each participant. 3.3.6. Fatigue protocol To induce fatigue, the participant performed the sit-to-stand task, with arms across the chest region from a chair (Helbostad et al., 2007), with the speed controlled by a metronome (30 beats/min). So, the cycle of sitting to standing and back to sitting was performed in 2 s. A standard chair (43 cm in height, 41 cm in width, 42 cm in depth) without arm rests was used for all participants. The instruction given to the participants was: stand up to an upright position with your knees fully extended, then sit back down and repeat this at the beat of the metronome until you can no longer perform the task. The fatigue protocol was stopped and it was assumed that the leg muscles were fatigued when the subject indicated not to be able to continue the task, or when the subject no longer performed at the desired movement frequency, or after 30 min. The time between the fatigue protocol and the gait trials (< 3 min) was expected not to allow full recovery (Parijat et al., 2008b). 3.3.7. Data analysis All the data were digitally filtered using zero-lag Butterworth filter. Kinematic data were filtered with a 5th order low-pass filter with cutoff frequency of 6Hz. Kinetic data were filtered with 4th order filter with cutoff frequency of 16Hz, and the magnitude of the ground reaction force was normalized by body weight. For free and adaptive gait (approach phase), the stride length, step width, stride duration, single and double support duration, speed in the stride (stride length divided by stride duration), maximum braking and propulsive vertical and anterior-posterior forces, and braking latency time (time between the foot contact with the ground and the maximum braking force) of the vertical forces were measured. For adaptive gait trials, step length, step width, step duration, single and double support duration and speed for the obstacle crossing and N+1 steps, the foot-obstacle distance before and after obstacle crossing, and toe-clearance for the leading and trailing limbs were calculated. Moreover, the maximum force in the maximum voluntary contractions and the endurance time in the fatigue protocol were measured. 27 3.3.8. Statistical analysis The dependent variables of interest were statistically analyzed with SPSS 15.0 for Windows® (α <0.05). The data were normally distributed, verified by the Shapiro-Wilk test. To verify the similarity between groups, the anthropometric characteristics, age, Multidimensional Fatigue Inventory values, maximum force and kinematic and kinetic variables before fatigue induction were compared through the Student t test for independent groups. The same statistical test was used to compare the endurance times between groups. To verify the development of fatigue, the Student t test for paired samples was applied on the maximum force values before and after the fatigue protocol for each group. The dependent variables of free and adaptive gait were compared using MANOVAs. One MANOVA was used for kinematic data of free gait and the approach phase of adaptive gait, with as independent variables level of physical activity (active and inactive), fatigue (before and after) and task (free and adaptive gait), with repeated measures over the last two factors. A similar MANOVA was used for kinetic data of the first force platform. The third MANOVA was for the kinetic data of the second force plate in adaptive gait and had level of physical activity and fatigue as independent variables, with repeated measures over fatigue. Similarly two MANOVAs were performed for kinematics of obstacle crossing and step N+1. When MANOVA revealed a main effect, univariate analyses were used to locate the differences. 3.4. Results The active and inactive groups were similar for age, anthropometric characteristics, muscle strength, fatigue level (Table 3.1) and different only with respect to body fat percentage (t1,8=-3.3, p<0.01). The fatigue protocol did induce fatigue in both groups as demonstrated by the lower maximum voluntary forces (active individuals: t1,9=4.1, p<0.01; inactive individuals: t1,9=2.6, p<0.01). Among the active participants, four individuals performed for the full 30 min; among the inactive participants none completed the full 30 min. Mean endurance time was shorter in the inactive individuals (Table 1; t1,8=2.4, p<0.02). 28 Table 3.1. Mean and standard deviation of the general characteristics, anthropometric measure, scores on the Multidimensional Fatigue Inventory and Habitual Physical Activity, maximal isometric force before (pre) and after (post) induction to fatigue and endurance time to fatigue for each group. * pre ≠ post; + active group ≠ inactive group. Group Variables Active (n=10) Inactive (n=10) Age (months) 296.5 ± 34.2 296.9 ± 35.4 Weight (kg) 73.2 ± 4.4 82.7 ± 17.6 Height (cm) 178.7 ± 10.1 178.8 ± 5.6 Percentage of body fat 9.6 ± 4.1+ 20.1 ± 8.9 Multidimensional Fatigue Inventory (points) 47.5 ± 5.6 46.9 ± 10.3 Habitual Physical Activity (points) 10.4 ± 1.49+ 5.9 ± 1.2 Maximal isometric force (N) pre 3346.7 ± 1002.3* 3099.1 ± 1351.9 post 2923.2 ± 1132.4* 2730.8 ± 1302.1 Endurance time to fatigue (s) 1018.4 ± 697.4+ 416.4 ± 381.7 Before fatigue, the groups were similar for all gait variables. Analysis of the kinematics of free gait and the approach phase in adaptive gait revealed main effects of task (Wilks' Lambda=0.58, F7,12=27.70, p<0.01) and fatigue (Wilks' Lambda=0.33, F7,12=3.40, p<0.03) only. For task (Table 3.2), univariate analyses indicated that free gait coincided with shorter stride durations (F1,18=9.95, p<0.01) and double support duration (F1,18=107.08, p<0.01), larger stride length (F1,18=23.58, p<0.01), higher speed (F1,18=23.56, p<0.01) and longer single support duration (F1,18=5.83, p<0.02). With respect to fatigue (Table 3.3), univariate analyses showed that fatigue coincided with increased step width (F1,18=18.11, p<0.01) and speed (F1,18=10.09, p<0.01), and decreased single support (F1,18=6.58, p<0.01) and stride durations (F1,18=10.89, p<0.01). For the kinetic data of free gait and adaptive gait, the MANOVA indicated an effect of task (Wilks’ Lambda=0.09, F7,12=16.114, p<0.01) and fatigue (Wilks’ Lambda=0.29, F7,12=4.17, p<0.01). Specifically for task (Table 3.2), the univariate analyses showed that adaptive gait coincided with greater maximum braking and propulsive vertical forces (F1,18=114.70, p<0.01 and F1,18=22.07, p<0.01) as well as greater maximum braking and propulsive anterior-posterior forces (F1,18=89.31, p<0.01 and F1,18=24.29, p<0.01). For fatigue (Table 3.4), the analysis indicated that fatigue coincided with a lower vertical maximum braking force (F1,18=5.55, p<0.03). 29 Table 3.2.Mean and standard deviation of the free and adaptive gait variables. Kinematics variable of approach phase and kinetic variables. BW – body weight. # free gait ≠ adaptive gait. Dependent variables Free gait Adaptive gait stride length (cm) 135.91±11.74# 131.30±10.50 step width (cm) 12.10±2.70 12.57±2.91 single support duration (s) 0.77±0.05# 0.75±0.07 double support duration (s) 0.29±0.4# 0.35±0.04 stride duration (s) 1.07±0.08# 1.11±0.10 stride speed (cm/s) 127.21±17.17# 119.22±14.27 maximum braking vertical force (BW) 1.08±0.07# 1.20±0.08 maximum propulsive vertical force (BW) 1.11±0.05# 1.17±0.05 braking latency time of vertical force (ms) 0.18±0.02# 0.16±0.02 maximum braking anterior-posterior force (BW) 0.15±0.03# 0.20±0.04 maximum propulsive anterior-posterior force(BW) 0.19±0.03# 0.24±0.04 Concerning obstacle crossing and N+1 variables (Table 3), the MANOVAs showed an effect of fatigue (Wilks’ Lambda=0.14, F10,9=5.38 p<0,01 and Wilks’ Lambda=0.31, F6,13=4.64, p<0,01). For obstacle crossing and N+1, univariate analyses revealed that fatigue coincided with a larger step width (F1,18=6.37, p<0.01 and F1,18=27.33, p<0.01), shorter double support time (F1,18=7.51, p<0.01 and F1,18=16.33, p<0.01), and higher speed (F1,18=5.35, p<0.03 and F1,18=8.34, p<0.01). In addition, for N+1 only we found a shorter step duration (F1,18=6.55, p<0.02) after fatigue. In the kinetic data of the force platform after the obstacle (Table 3.4), the MANOVAs showed an effect of physical activity level (Wilks’ Lambda=0.35, F7,12=3.09 p<0,04). The univariate analyses showed that inactive individuals produced a higher maximum braking anterior-posterior force (F1,18=7.1, p<0.01) and maximum propulsive vertical force (F1,18=6.42, p<0.02). 1 T ab le 3 .3 .M ea n an d st an da rd d ev ia tio n of s pa tia l a nd te m po ra l p ar am et er s ac co rd in g to fa tig ue (i nd ep en de nt ly ta sk a nd p hy si ca l a ct iv ity le ve l) an d ph ys ic al a ct iv ity le ve l ( in de pe nd en tly ta sk a nd fa tig ue ). K in em at ic v ar ia bl es o f f re e ga it/ ap pr oa ch p ha se , c ro ss in g ob st ac le (N ) a nd s te p af te r cr os si ng (N +1 ). LL – le ad in g lim b; T L – tra ili ng li m b. * p re (b ef or e fa tig ue ) ≠ p os t ( af te r f at ig ue ). D ep en de nt v ar ia bl es M om en ts Pr e Po st A ct iv e In ac tiv e st rid e/ st ep le ng th (c m ) fr ee /a pp ro ac h N 13 5. 66 ±1 1. 71 71 .6 7± 8. 01 13 0. 82 ±1 0. 57 72 .7 9± 7. 17 13 2. 65 ±8 .7 2 73 .5 5± 7. 28 13 4. 55 ±1 3. 77 70 .9 4± 8. 49 N +1 65 .2 2± 6. 27 66 .5 2± 7. 08 63 .7 0± 7. 48 68 .0 4± 6. 63 st ep w id th (c m ) fr ee /a pp ro ac h N 11 .4 8± 2. 51 * 10 .5 8± 2. 67 * 11 .8 0± 2. 70 12 .8 0± 3. 06 11 .9 7± 3. 09 11 .9 6± 3. 18 12 .7 0± 2. 94 11 .4 1± 4. 08 N +1 14 .2 2± 4. 36 * 16 .1 1± 6. 02 14 .3 2± 5. 47 16 .0 1± 5. 46 si ng le su pp or t d ur at io n (s ) fr ee /a pp ro ac h N 0. 78 ±0 .0 6* 0. 42 ±0 .0 5 0. 76 ±0 .0 7 0. 42 ±0 .0 6 0. 78 ±0 .0 4 0. 43 ±0 .0 4 0. 74 ±0 .0 7 0. 40 ±0 .0 6 N +1 0. 50 ±0 .0 6 0. 50 ±0 .0 6 0. 50 ±0 .0 5 0. 50 ±0 .0 8 do ub le su pp or t d ur at io n (s ) fr ee /a pp ro ac h N 0. 30 ±0 .0 4 0. 20 ±0 .0 4* 0. 35 ±0 .0 4 0. 18 ±0 .0 4 0. 32 ±0 .0 4 0. 19 ±0 .0 4 0. 32 ±0 .0 6 0. 20 ±0 .0 6 N +1 0. 16 ±0 .0 2* 0. 15 ±0 .0 2 0. 16 ±0 .0 2 0. 15 ±0 .0 3 st rid e/ st ep d ur at io n (s ) fr ee /a pp ro ac h N 1. 08 ±0 .0 9* 0. 62 ±0 .0 9 1. 12 ±0 .1 0 0. 61 ±0 .0 7 1. 11 ±0 .0 8 0. 63 ±0 .0 7 1. 07 ±0 .1 1 0. 60 ±0 .1 1 N +1 0. 67 ±0 .0 7* 0. 65 ±0 .0 7 0. 66 ±0 .0 7 0. 66 ±0 .0 9 st rid e/ st ep sp ee d (c m /s ) fr ee /a pp ro ac h N 12 1. 60 ±1 5. 81 * 11 7. 66 ±2 8. 37 * 12 4. 83 ±1 6. 62 12 4. 66 ±3 6. 33 11 9. 49 ±1 1. 96 11 7. 14 ±1 9. 24 12 6. 93 ±1 9. 58 12 5. 18 ±2 8. 18 N +1 98 .8 8± 15 .6 2* 10 3. 80 ±1 8. 62 96 .9 1± 18 .2 3 10 6. 43 ±1 8. 26 fo ot -o bs ta cl e di st an ce b ef or e ob st ac le - LL (c m ) N 11 2. 66 ±1 0. 13 11 3. 96 ±9 .7 5 11 2. 43 ±8 .8 8 11 3. 98 ±1 3. 00 to e- cl ea ra nc e - L L (c m ) N 9. 09 ±3 .0 1 9. 38 ±2 .9 1 8. 36 ±2 .4 0 10 .0 6± 3. 78 fo ot -o bs ta cl e di st an ce a fte r o bs ta cl e - L L (c m ) N 24 .2 2± 4. 78 24 .4 2± 5. 24 24 .9 1± 6. 30 23 .7 3± 6. 15 fo ot -o bs ta cl e di st an ce b ef or e ob st ac le - TL (c m ) N 48 .1 8± 6. 19 48 .4 1± 6. 36 49 .6 8± 6. 45 46 .7 7± 8. 08 to e- cl ea ra nc e - T L (c m ) N 31 .2 8± 3. 64 30 .1 6± 4. 59 29 .6 5± 5. 85 31 .6 5± 4. 67 fo ot -o bs ta cl e di st an ce a fte r o bs ta cl e - T L (c m ) N 89 .6 2± 8. 64 91 .0 5± 10 .3 7 88 .8 1± 11 .2 9 91 .7 8± 10 .1 9 30 31 3.5. Discussion The aim of this study was to analyze the effect of muscle fatigue in active and inactive young adults on the kinematic and kinetic parameters of free and adaptive gait. The expectations of the study were confirmed in part, by showing that muscle fatigue interferes with spatial-temporal and kinetic parameters of free and adaptive gait, but fatigue effects were not different between active and inactive individuals. Active young adults showed greater endurance in the fatigue induction protocol than inactive young adults. Furthermore, the changes in the spatial-temporal gait parameters with fatigue were independent of the type of gait. The adjustments in adaptive gait compared to free gait consisted of increased stride and double support durations and decreased stride length, single support duration and stride speed. This speed modulation appears to be caused by a larger magnitude of the negative horizontal (braking) force in the last stride before crossing the obstacle. Locomotion in complex environments requires adaptive ability from the locomotor system (Krell and Patla, 2002) and more attention (Bradshaw and Sparrow, 2001), especially when crossing an obstacle (Gobbi et al., 2011; Silva et al., 2011). Reduced speed allows more exploration and collection of relevant information and more time for planning the action (Tresilian, 2004). The decreased step length, gait speed and stride duration appear to disclose the use of such proactive mechanisms for modulation of the effector system according to the perceived environmental characteristics (Gerin-Lajoie et al., 2005) and an anticipatory strategy to guarantee dynamic stability during obstacle crossing (Patla, 2003). From this perspective, we expected more pronounced changes with fatigue in adaptive gait than in free gait, which were, however, not observed. 59 T ab le 3 .4 .M ea n an d st an da rd d ev ia tio n of k in et ic p ar am et er s ac co rd in g fa tig ue ( in de pe nd en tly ta sk a nd p hy si ca l a ct iv ity le ve l) an d ph ys ic al ac tiv ity le ve l ( in de pe nd en tly ta sk a nd fa tig ue ). K in et ic v ar ia bl es o f f re e ga it/ ap pr oa ch p ha se a nd c ro ss in g ob st ac le (N ). * pr e (b ef or e fa tig ue ) ≠ po st (a fte r f at ig ue ); + ac tiv e gr ou p ≠ in ac tiv e gr ou p. D ep en de nt v ar ia bl es M om en ts Pr e Po st A ct iv e In ac tiv e m ax im um b ra ki ng v er tic al fo rc e (B W ) fr ee /a pp ro ac h N 1. 15 ±0 .0 9* 1. 15 ±0 .1 1 1. 12 ±0 .1 0 1. 12 ±0 .0 8 1. 13 ±0 .1 0 1. 11 ±0 .0 9 1. 14 ±0 .1 0 1. 16 ±0 .1 1 m ax im um p ro pu ls iv e ve rti ca l f or ce (B W ) fr ee /a pp ro ac h N 1. 15 ±0 .0 6 1. 10 ±0 .0 6 1. 14 ±0 .0 6 1. 10 ±0 .0 7 1. 13 ±0 .0 6 1. 07 ±0 .0 7+ 1. 16 ±0 .0 7 1. 13 ±0 .1 2 br ak in g la te nc y tim e of v er tic al fo rc e (m s) fr ee /a pp ro ac h N 0. 17 ±0 .0 2 0. 17 ±0 .0 3 0. 17 ±0 .0 3 0. 16 ±0 .0 4 0. 17 ±0 .0 2 0. 17 ±0 .0 3 0. 17 ±0 .0 3 0. 17 ±0 .0 4 m ax im um b ra ki ng a nt er io r- po st er io r f or ce (B W ) fr ee /a pp ro ac h N -0 .1 8± 0. 04 -0 .2 6± 0. 09 -0 .1 7± 0. 04 -0 .2 5± 0. 09 -0 .1 6± 0. 04 -0 .2 2± 0. 03 + -0 .1 9± 0. 04 -0 .2 6± 0. 02 m ax im um p ro pu ls iv e an te rio r- po st er io r f or ce (B W ) fr ee /a pp ro ac h N 0. 22 ±0 .0 4 0. 13 ±0 .1 0 0. 21 ±0 .0 4 0. 15 ±0 .1 0 0. 20 ±0 .0 4 0. 12 ±0 .0 3 0. 23 ±0 .0 4 0. 14 ±0 .0 3 32 33 The fatigue protocol used can be expected to mainly affect the quadriceps muscles. Indeed, knee extension strength was reduced after the fatigue protocol. Reduced strength after exercise is considered the indication of muscle fatigue in accordance with its definition as a loss of force generating capacity (Katsiaras et al., 2005; Bigland-Ritchie and Woods, 1984). The decrease of the maximum vertical force in the braking phase in both tasks may be a consequence of this loss of force producing capacity, through decreased knee stiffness during weight acceptance. Moreover, in the approach phase of stepping down, we found that quadriceps muscle fatigue coincided with a decreased muscle activity of the quadriceps muscle (Barbieri et al., 2012c). Quadriceps fatigue adversely affects knee proprioception (Bigland-Ritchie and Woods, 1984), postural control in single leg stance (Paillard et al., 2010), and has been associated with an increased risk of falling (Parijat and Lockhart, 2008a,b; Lattanzio et al., 1997). Modulations in performance with fatigue were not task- dependent. One possible explanation is that, despite that individuals did need to adjust their gait when the obstacle was present, this task is not very challenging for young adults. Possibly fatigue of another muscular group or a more challenging adaptive task could show different results. The participants in this study appeared to seek more stability during gait after the fatigue protocol than before. They increased step widths in both free and adaptive gait as was previously demonstrated in elderly adults in free gait (Helbostad et al., 2007). Increased step width provides a larger margin of safety in controlling medio-lateral movements of the body’s center of mass (Hof et al., 2007). Participants also reduced stride durations and related variables, such as durations of single and double support, as well as braking forces, irrespective of the type of task. Reduced step duration, facilitates control of the body center of mass in the fore-aft direction (Hof et al., 2007; Hof et al., 2005) and appears to be the preferred strategy to deal with balance threats (Hak et al., 2012) even if this coincides with an increased speed (Brujin et al., 2009) as was the case in the present study. In line with the present results, increased gait speed with fatigue was found in older people (Granacher et al., 2010). This may be a direct consequence of the reduction in step duration. On the other hand participants may have tried to perform the task as quickly as possible (Granacher et al., 2010) and the increase in speed could be a risky strategy that decreases the reaction and processing time required to cross the obstacle (Gobbi et al., 2011; Silva et al., 2011; Tresilian, 2004), which may be compensated for by larger step width (Helbostad and Moe-Nilssen, 2003). Previous authors have suggested that muscle fatigue increases fall risk (Parijat and Lockhart, 2008a,b), however this was based on an increased heel contact velocity, which mainly relates 34 to the risk of slipping. In the present study, we did not find a decrease in braking latency time, which would indicate a less safe weight transfer to the new stance leg. Furthermore, toe- clearance, the most obvious indicator of the risk of tripping in the adaptive gait task, did not change with fatigue in either leg.� Active and inactive young adults showed almost the same behavior before and after muscle fatigue. The active group had a better muscular capacity, as reflected by the longer endurance times. However, muscle strength before and after fatigue was not different between groups. A similar general locomotor strategy for active and inactive young adults was previously found in free gait and adaptive gait (Niang and McFadyen, 2005). However, gait speed and speed of the leading leg in crossing an obstacle were higher in the active participants (Niang and McFadyen, 2005). In the present study, the only difference between groups was found also for the leading leg in t