AGE (2016) 38: 57 DOI 10.1007/s11357-016-9921-2
Effects of age and sex on neuromuscular-mechanical determinants of muscle strength Rui Wu & Eamonn Delahunt & Massimiliano Ditroilo & Madeleine Lowery & Giuseppe De Vito
Received: 4 February 2016 / Accepted: 8 May 2016 / Published online: 17 May 2016 # American Aging Association 2016
Abstract The aim of this study was to concurrently assess the effect of age on neuromuscular and mechanical properties in 24 young (23.6 ± 3.7 years) and 20 older (66.5 ± 3.8 years) healthy males and females. Maximal strength of knee extensors (KE) and flexors (KF), contractile rate of torque development (RTD) and neural activation of agonist-antagonist muscles (surface EMG) were examined during maximal voluntary isometric contraction (MVIC). Tissue stiffness (i.e. musculo-articular stiffness (MAS) and muscle stiffness (MS)) was examined via the free-oscillation technique, whereas muscle architecture (MA) of the vastus lateralis and subcutaneous fat were measured by ultrasonography. Males exhibited a greater age-related decline for KE (47.4 %) and KF (53.1 %) MVIC, and RTD (60.4 %) when compared to females (32.9, 42.6 and 34.0 %, respectively). Neural activation of agonist muscles during KE MVIC falls markedly with ageing; however, no age and sex effects were observed in the antagonist co-activation. MAS and MS were lower in elderly
R. Wu (*) : E. Delahunt : M. Ditroilo : G. De Vito School of Public Health, Physiotherapy and Sports Science, University College Dublin, Dublin, Republic of Ireland e-mail: [email protected] E. Delahunt : M. Ditroilo : G. De Vito Institute for Sport and Health, University College Dublin, Dublin, Republic of Ireland M. Lowery School of Electrical, Electronic and Communications Engineering, University College Dublin, Dublin, Republic of Ireland
compared with young participants and in females compared with males. Regarding MA, main effects for age (young 23.0 ± 3.3 vs older 19.5 ± 2.0 mm) and sex (males 22.4 ± 3.5 vs females 20.4 ± 2.7 mm) were detected in muscle thickness. For fascicle length, there was an effect of age (young 104.6 ± 8.8 vs older 89.8 ± 10.5 mm), while for pennation angle, there was an effect of sex (males 13.3 ± 2.4 vs females 11.5 ± 1.7°). These findings suggest that both neuromuscular and mechanical declines are important contributors to the age-related loss of muscle strength/ function but with some peculiar sex-related differences. Keywords Ageing . Sex . Muscle strength . Muscle architecture . Stiffness
Introduction Deterioration in muscle strength/function is an inevitable consequence of the normal ageing process and can be associated with functional limitations and participation restrictions, such as an increased risk of falls (Wolfson et al. 1995), hip fractures (Langlois et al. 1998) and a loss of bone mineral density (Sinaki et al. 1986), making elderly persons more dependent on others in daily life. This is particularly relevant to females, who live longer, reach the threshold of dependence earlier and have lower physical capacities than males at all ages (Larsson et al. 1979; Lindle et al. 1997). Loss of muscle mass represents the main factor associated with decreased muscle strength/function in elderly
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persons. This phenomenon is attributed to reductions in both the number and size of individual muscle fibres, especially type II fibres (Frontera et al. 2000; D’Antona et al. 2003). On the other hand, it is well known that muscle strength declines at a greater rate than muscle mass during the normal ageing process (Young et al. 1985; Jubrias et al. 1997). This disproportionate loss indicates that other variables are likely to contribute to the age-related deterioration in muscle strength/function, with both mechanical and neuromuscular factors requiring consideration. Changes in muscle architecture (MA) have been associated with decreased muscle strength/ function in elderly persons (Kubo et al. 2003a; Narici et al. 2003; Strasser et al. 2013). Other relevant mechanical factors include tissue stiffness characteristics, which have been investigated in different biological structures (e.g. tendon, muscle and joint) involved in characteristic locomotion (Reeves et al. 2003; Bojsen-Moller et al. 2005; Ditroilo et al. 2012). Age-related decrease in muscle strength/function depends also on alterations in neural drive to agonist and antagonist muscles (Izquierdo et al. 1999; Macaluso et al. 2002; Macaluso and De Vito 2004). A number of studies have reported that maximal voluntary neural activation of agonist muscles was lower in groups of elderly individuals when compared to young and middle-aged groups (Häkkinen et al. 1998a; Macaluso et al. 2002; Billot et al. 2014). Ideally, to thoroughly investigate age-related decline in muscle strength/function, the changes manifest in both mechanical and neuromuscular factors should be concurrently quantified and assessed. To the best of our knowledge, no studies to date have concomitantly examined and contrasted age-related deterioration in muscle strength/ function with respect to the contribution of MA, tissue stiffness and neural activities of agonist-antagonist
muscles. Therefore, the aim of the present study was to simultaneously assess the age-related modifications of the aforementioned neuromuscular-mechanical factors by comparing young and older adults of both sexes.
Materials and methods Participants Twenty-four young adults (11 males and 13 females) and 20 older adults (11 males and 9 females) volunteered to participate in the study. The criteria for exclusion were applied through a general medical questionnaire based on the definition of ‘medically stable’ as proposed by Greig et al. (1994). Participants were excluded primarily for the following conditions: presence or/and history of cardiovascular, cerebrovascular, neurological, uncontrolled metabolic, respiratory and major systemic diseases. None of the participants had previously engaged in strength training or competitive sports within the last 5 years. In order to determine the reliability for the variables of interest, participants attended the laboratory on two occasions separated by at least 1 week. Each laboratory visit lasted approximately 2 h, with the same order of testing undertaken on both days: maximal voluntary isometric contraction (MVIC) of both the knee extensors (KE) and flexors (KF), musculo-articular stiffness (MAS) and muscle stiffness (MS), and MA. The study was approved by the University Human Research Ethic Committee, and all participants provided written informed consent to the procedures and aims of the study. The age and the main physical characteristics of participants are reported in Table 1.
Table 1 Participants characteristics Young
Older
Main effect
Interaction effect
Male YM (n = 11)
Female YF (n = 13)
Male OM (n = 11)
Female OF (n = 9)
Age p value
Sex p value
Age (year)
23.7 ± 4.2
23.5 ± 3.4
66.8 ± 3.4
66.1 ± 4.4
Effects of age and sex on neuromuscular-mechanical determinants of muscle strength Rui Wu & Eamonn Delahunt & Massimiliano Ditroilo & Madeleine Lowery & Giuseppe De Vito
Received: 4 February 2016 / Accepted: 8 May 2016 / Published online: 17 May 2016 # American Aging Association 2016
Abstract The aim of this study was to concurrently assess the effect of age on neuromuscular and mechanical properties in 24 young (23.6 ± 3.7 years) and 20 older (66.5 ± 3.8 years) healthy males and females. Maximal strength of knee extensors (KE) and flexors (KF), contractile rate of torque development (RTD) and neural activation of agonist-antagonist muscles (surface EMG) were examined during maximal voluntary isometric contraction (MVIC). Tissue stiffness (i.e. musculo-articular stiffness (MAS) and muscle stiffness (MS)) was examined via the free-oscillation technique, whereas muscle architecture (MA) of the vastus lateralis and subcutaneous fat were measured by ultrasonography. Males exhibited a greater age-related decline for KE (47.4 %) and KF (53.1 %) MVIC, and RTD (60.4 %) when compared to females (32.9, 42.6 and 34.0 %, respectively). Neural activation of agonist muscles during KE MVIC falls markedly with ageing; however, no age and sex effects were observed in the antagonist co-activation. MAS and MS were lower in elderly
R. Wu (*) : E. Delahunt : M. Ditroilo : G. De Vito School of Public Health, Physiotherapy and Sports Science, University College Dublin, Dublin, Republic of Ireland e-mail: [email protected] E. Delahunt : M. Ditroilo : G. De Vito Institute for Sport and Health, University College Dublin, Dublin, Republic of Ireland M. Lowery School of Electrical, Electronic and Communications Engineering, University College Dublin, Dublin, Republic of Ireland
compared with young participants and in females compared with males. Regarding MA, main effects for age (young 23.0 ± 3.3 vs older 19.5 ± 2.0 mm) and sex (males 22.4 ± 3.5 vs females 20.4 ± 2.7 mm) were detected in muscle thickness. For fascicle length, there was an effect of age (young 104.6 ± 8.8 vs older 89.8 ± 10.5 mm), while for pennation angle, there was an effect of sex (males 13.3 ± 2.4 vs females 11.5 ± 1.7°). These findings suggest that both neuromuscular and mechanical declines are important contributors to the age-related loss of muscle strength/ function but with some peculiar sex-related differences. Keywords Ageing . Sex . Muscle strength . Muscle architecture . Stiffness
Introduction Deterioration in muscle strength/function is an inevitable consequence of the normal ageing process and can be associated with functional limitations and participation restrictions, such as an increased risk of falls (Wolfson et al. 1995), hip fractures (Langlois et al. 1998) and a loss of bone mineral density (Sinaki et al. 1986), making elderly persons more dependent on others in daily life. This is particularly relevant to females, who live longer, reach the threshold of dependence earlier and have lower physical capacities than males at all ages (Larsson et al. 1979; Lindle et al. 1997). Loss of muscle mass represents the main factor associated with decreased muscle strength/function in elderly
57 Page 2 of 12
AGE (2016) 38: 57
persons. This phenomenon is attributed to reductions in both the number and size of individual muscle fibres, especially type II fibres (Frontera et al. 2000; D’Antona et al. 2003). On the other hand, it is well known that muscle strength declines at a greater rate than muscle mass during the normal ageing process (Young et al. 1985; Jubrias et al. 1997). This disproportionate loss indicates that other variables are likely to contribute to the age-related deterioration in muscle strength/function, with both mechanical and neuromuscular factors requiring consideration. Changes in muscle architecture (MA) have been associated with decreased muscle strength/ function in elderly persons (Kubo et al. 2003a; Narici et al. 2003; Strasser et al. 2013). Other relevant mechanical factors include tissue stiffness characteristics, which have been investigated in different biological structures (e.g. tendon, muscle and joint) involved in characteristic locomotion (Reeves et al. 2003; Bojsen-Moller et al. 2005; Ditroilo et al. 2012). Age-related decrease in muscle strength/function depends also on alterations in neural drive to agonist and antagonist muscles (Izquierdo et al. 1999; Macaluso et al. 2002; Macaluso and De Vito 2004). A number of studies have reported that maximal voluntary neural activation of agonist muscles was lower in groups of elderly individuals when compared to young and middle-aged groups (Häkkinen et al. 1998a; Macaluso et al. 2002; Billot et al. 2014). Ideally, to thoroughly investigate age-related decline in muscle strength/function, the changes manifest in both mechanical and neuromuscular factors should be concurrently quantified and assessed. To the best of our knowledge, no studies to date have concomitantly examined and contrasted age-related deterioration in muscle strength/ function with respect to the contribution of MA, tissue stiffness and neural activities of agonist-antagonist
muscles. Therefore, the aim of the present study was to simultaneously assess the age-related modifications of the aforementioned neuromuscular-mechanical factors by comparing young and older adults of both sexes.
Materials and methods Participants Twenty-four young adults (11 males and 13 females) and 20 older adults (11 males and 9 females) volunteered to participate in the study. The criteria for exclusion were applied through a general medical questionnaire based on the definition of ‘medically stable’ as proposed by Greig et al. (1994). Participants were excluded primarily for the following conditions: presence or/and history of cardiovascular, cerebrovascular, neurological, uncontrolled metabolic, respiratory and major systemic diseases. None of the participants had previously engaged in strength training or competitive sports within the last 5 years. In order to determine the reliability for the variables of interest, participants attended the laboratory on two occasions separated by at least 1 week. Each laboratory visit lasted approximately 2 h, with the same order of testing undertaken on both days: maximal voluntary isometric contraction (MVIC) of both the knee extensors (KE) and flexors (KF), musculo-articular stiffness (MAS) and muscle stiffness (MS), and MA. The study was approved by the University Human Research Ethic Committee, and all participants provided written informed consent to the procedures and aims of the study. The age and the main physical characteristics of participants are reported in Table 1.
Table 1 Participants characteristics Young
Older
Main effect
Interaction effect
Male YM (n = 11)
Female YF (n = 13)
Male OM (n = 11)
Female OF (n = 9)
Age p value
Sex p value
Age (year)
23.7 ± 4.2
23.5 ± 3.4
66.8 ± 3.4
66.1 ± 4.4
