| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Review Article |
1 Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, Alsager Campus, Hassall Road, Alsager, Cheshire ST7 2HL, UK
 |
Abstract |
|---|
 Top Abstract References |
|---|
(Received 28 November 2005;
accepted after revision 1 February 2006; first published online 9 February 2006)
Corresponding author N. D. Reeves: Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, Alsager Campus, Hassall Road, Alsager, Cheshire ST7 2HL, UK. Email: n.reeves{at}mmu.ac.uk
An ageing population
The proportion of adults over the age of 60 years currently represents one-fifth of the total population in the UK (The Office for National Statistics, 2001) and this is predicted to rise to one-third of the population by the year 2030 (data from the US census bureau and presented by McMurdo, 2000). A similar picture emerges worldwide, indicating that modern-day society will have to adapt to the wide-ranging challenges presented by an increasingly aged population. One of the major challenges for society will be the health-related consequences of ageing, since they could place an enormous burden upon the health services. Life expectancy has increased for males and females in the UK between the years of 1981 (life expectancy for males, 70.9 years; females, 76.8 years) and 2001 (life expectancy for males, 75.7 years; females, 80.4 years). However, the number of years lived in good health has not risen at the same rate, meaning that the extra years are largely spent in poor health (source: The Office for National Statistics, presented by Hebert, 2004). Falls are one of the leading causes of morbidity and mortality in old age, and muscular weakness is a major factor contributing to the occurrence of falls and general physical deconditioning (Whipple et al. 1987; Feder et al. 2000; Khan et al. 2001; Skelton et al. 2002). In fact, frailty in old age can impact upon many daily activities and contribute to a general reduction in the quality of life. Studies, however, have shown that resistance training can improve physical function in older adults (e.g. Sipila et al. 1996; Buchner et al. 1997; Robertson et al. 2001). The physical condition of older adults is therefore clearly a pertinent issue and one that has received much attention in recent years. This review will present current knowledge on myotendinous plasticity to ageing and the effects of resistance exercise interventions in old age, from the single-fibre level up to the whole muscle–tendon unit.
Cellular and molecular determinants of sarcopenia
One of the most noticeable consequences of ageing is the loss of muscle mass. This phenomenon, known as sarcopenia, is the result of molecular, cellular, nutritional and hormonal changes. From 20 to 80 years of age, 
30% of muscle mass is lost (Young et al. 1985). This decrease in muscle mass is due both to a reduction in the size and a decrease in the number of muscle fibres, particularly in individuals aged 70 and above (Lexell et al. 1988; Lexell, 1995). However, because of motor unit remodelling, denervated muscle fibres (mostly of type II), are reinnervated by sprouting of collateral branches of the 
-motoneurones of the surviving motor units (predominantly of type I), leading to the formation of giant slow-twitch motor units. Also, because of the reduction in the total number of fibres, the mechanical load sustained by each fibre is increased and, as a result, compensatory fibre hypertrophy is frequently observed (Alnaqeeb & Goldspink, 1987). In contrast with earlier reports of a selective loss of fast-twitch fibres, recent data have shown that the proportion of type I and type II fibres is generally maintained in old age. This apparent controversy is probably due to the fact that the previous investigations were based on histochemical identification of fibre types (Trappe et al. 2004). This may have lead to misclassification of fibre types, since this technique does not enable precise identification of fibres coexpressing more than one MHC (hybrid fibres). Recently, however, MHC analysis by gel electrophoresis on single fibres, rather than on homogenates, has shown that muscles of elderly people contain a high proportion (52%) of hybrid fibres, most of which are either type I/IIA (28%) or IIA/IIX (22%; Andersen et al. 1999; Andersen, 2003), while the expression of the fastest isoform (IIX) is very low, being 0.3–1.3% of the total fibre population (Andersen et al. 1999; Williamson et al. 2000). The picture is far from simple, however, since myosin isoform composition is affected both by ageing and by a reduction in physical activity level, common in old age (e.g. Morse et al. 2004), which have conflicting effects. In fact, whereas ageing in healthy active individuals tends to maintain unaltered the proportion of slow myosin isoforms (MHC-1), a decrease in physical activity level leads to a reduction of the expression of MHC-1 isoform while increasing that of the IIX and IIAX hybrid isoforms (D'Antona et al. 2003). Hence, when considering myosin heavy chain expression, it is very difficult to disentangle the effects of ageing per se from those of reduced physical activity level. What can be concluded in general is that ageing does not lead to the loss of a particular type of muscle fibre; rather, the loss seems unselective, as evidenced by an increased proportion of fibres coexpressing more than one isoform, the proportion of which, however, is affected both by ageing and disuse.
These conclusions may appear in contradiction with the common observation of slower twitch contraction and relaxation times of elderly muscle (e.g. Narici et al. 1991). This apparent paradox may be partly explained by the finding that the maximum shortening speed, measured by in vitro motility assays, of fast and slow myosin molecules of muscle fibres of elderly individuals is in fact lower than that of young subjects (Hook et al. 2001). Considering, however, that this phenomenon mainly concerns the maximum shortening speed of type I fibres while that of the type IIA fibres is unaffected (Hook et al. 2001), it seems probable that the overall effect on the maximum shortening velocity of whole muscle may be small. However, two other factors may account for this discrepancy: one is an impairment of excitation–contraction (E–C) coupling; the other is a decrease in tendon stiffness. Experiments by Delbono (2000) indicate that E–C processes become uncoupled in old age due to a reduction in T-tubule dihydropyridine receptors (DHPR) and in sarcoplasmic reticulum (SR) membrane receptors. This phenomenon leads to an increased proportion of SR calcium release channels or ryanodine receptors uncoupled to DHPR, which may result in failure of the transduction of sarcolemmal depolarization into a calcium signal and a mechanical response. The reason why a decrease in tendon stiffness may also contribute to the slowing down of muscle contraction when measured in vivo and in toto conditions resides on the notion that contraction speed depends on the force–velocity properties of the contractile component as well as on the compliance of the series elastic component, of which the tendon is the main part. Since, in old age, tendon compliance increases (Maganaris, 2001; Onambéléet al. 2006), a longer time will be needed to stretch the tendon, with the result that less force will be produced over a set time. The molecular mechanisms at the basis of sarcopenia are not yet fully understood, but the prevailing theory is that increased levels of reactive oxygen species (ROS), resulting from decreased levels of superoxide dismutase, lead to cellular damage and eventually to cell death by apoptosis (Dirks & Leeuwenburgh, 2005). Cell apoptosis, however, may also be triggered by elevated expression of inhibitors of differentiation proteins (Id), as observed in old rats (Alway et al. 2002). In old age, repair of muscle fibre damage caused by ROS attack or by elevated Id levels is reduced because of decreased proliferation and differentiation of satellite cells; therefore, both cellular damage and failure of the repair processes contribute to sarcopenia. The resulting muscle weakness is not only due to simple fibre atrophy and hypoplasia, but also to a reduction in the intrinsic force of single fibres (specific tension). This decline in single-fibre specific tension associated with ageing has been found in both human and animal muscle (Brooks & Faulkner, 1988; Larsson et al. 1997) and seems to originate both from a decrease in the number of cross-bridges (as suggested by a decrease in myofibrillar protein density) rather than in the force exerted by each cross-bridge (D'Antona et al. 2003), and from a reduction in E–C coupling (Delbono, 2000).
Muscle architecture: fundamental concepts
The geometric arrangement of muscle fibres within a muscle is a major determinant of the muscle's functional properties (e.g. Gans & Bock, 1965). Two important architectural characteristics are the fibre length and physiological cross-sectional area (PCSA) of the muscle. Fibre length reflects the number of in-series sarcomeres in the fibres of the muscle and is therefore proportional to the contractile velocity and excursion range. The PCSA is the sum of cross-sectional areas of all fibres in a muscle (Fig. 1). It is therefore a measure of the number of in-parallel sarcomeres in the muscle and is proportional to the force-generating potential of the muscle. PCSA can be calculated as:
|
| (1) |
is the pennation angle of the muscle, i.e. the angle of the muscle fibres in relation to the muscle's line of pull. From this equation it appears as if pennation angle ‘penalizes’ maximum force generation. This is not the case, however, because although pennation angle decreases the effective contractile force vector transmitted to the tendon, it also allows more contractile material to be placed in parallel along the tendon (Fig. 1). There is a trade off between the two effects, but providing pennation angle is not greater than 45 deg, in theory for a given muscle volume, the contractile force-generating potential of the whole muscle increases with increasing pennation angle (Alexander & Vernon, 1975). Experimental models of muscle hypertrophy in young adults support the notion that an increase in pennation angle occurs to accommodate an increase in contractile material (Kawakami et al. 1993; Aagaard et al. 2001).
|
Influence of ageing on muscle architecture
One of the major musculoskeletal factors characterizing ageing is muscle atrophy, which at the level of the whole muscle has typically been quantified in terms of anatomical cross-sectional area (ACSA), i.e. a cross-section at right angles to the muscle's line of action and not necessarily to the direction of the muscle fibres. Senile sarcopenia affecting various muscle groups is evident from cross-sectional studies showing that muscle size is 20% smaller in older adults compared to young adults (Klein et al. 2001; Narici et al. 2003; Morse et al. 2004). The measurement of gross muscle area provides a useful indication of the decreasing contractile area with ageing, but it does not directly represent the decline in force-producing potential because other intramuscular factors will also be affected by ageing. The amount of intramuscular non-contractile material has been found to increase with ageing and would cause overestimations of the actual contractile area (Kent-Braun & Ng, 1999; Kent-Braun et al. 2000; Macaluso et al. 2002).
Non-contractile material has been quantified using MRI signal intensity analysis. This technique is based on the principle that fat tissue has a very high signal intensity, connective tissue has a very low signal intensity and the signal intensity of muscle lies between the two. This method is associated with some inherent limitations; for example, it is not possible to ascertain whether an MRI signal intensity value is higher because of increases in fat tissue or because of reductions in the amount of connective tissue, or indeed both. Hence, it is difficult to determine relative changes in the individual elements of the non-contractile component with this method. Intramuscular connective tissue can be qualified from muscle samples using a tissue staining technique. By applying this technique, older animals have been found to have greater amounts of intramuscular connective tissue compared to younger animals (Alnaqeeb et al. 1984). The connective tissue changes in animal muscle were implicated in alterations to both active and passive force components. Further work is required to elucidate the specific changes in human intramuscular connective tissue with ageing.
In addition to the amount of intramuscular non-contractile material, muscle architecture is another factor that is modified with ageing. Cross-sectional comparisons of young and older humans have shown that fascicles are shorter by 10–16% in the gastrocnemius muscle of the elderly (Kubo et al. 2003a; Narici et al. 2003; Morse et al. 2005a). In addition, pennation angles in the gastrocnemius muscle are smaller by 7–16% in the elderly (Kubo et al. 2003a; Narici et al. 2003; Morse et al. 2005a; Fig. 2). The physiological manifestations of ageing may not always be caused solely by the ageing process, but may also be influenced by reduced use. However, the participants in the study of Narici et al. (2003) were matched for physical activity levels and so represent true ageing effects as closely as possible. These ageing-induced modifications of muscle architecture indicate that senile sarcopenia quantified from muscle ACSA or volume measurements alone may not validly represent the reduced force-producing capacity with ageing. For example, gastrocnemius muscle volume is smaller in elderly men by 25–28% compared to young adult men, whilst the PCSA of this muscle is smaller by 15–16% in the elderly (Narici et al. 2003; Morse et al. 2005a,c).
|
However, the operating range of in vivo muscles is also influenced by the stiffness of the in-series elastic structures and in particular the free tendon. This is because the extent of muscle fibre shortening depends upon the degree of tendon elongation. Thus, whilst ageing-related changes in the structure and function of the muscle itself must be understood, the properties of other musculoskeletal structures, such as the tendon, also need to be considered when evaluating the performance of the whole muscle–tendon unit.
Tendon mechanical properties: fundamental concepts and the influence of ageing
In vitro studies show that, similar to muscles, tendons are also altered by ageing (for reviews see Butler et al. 1978; Viidik, 1982; Tuite et al. 1997; Kjaer, 2004). However, the in vitro experiments aimed to characterize the effect of ageing on tendon mechanical properties show inconsistent results. Some studies (Shadwick, 1990) show that ageing makes the tendinous material stiffer (material stiffness, or Young's modulus, is the slope of the tensile force versus elongation normalized to the dimensions of the tendon; Fig. 3), stronger (strength is the maximum load that the specimen can withstand before it breaks) and more rebound resilient (rebound resilience equals 100% minus the mechanical hysteresis [%]; it reflects the ability of the tendon to return elastic strain energy on recoil). Other studies, however, report opposite results (Vogel, 1980, 1983; Blevins et al. 1994; Nakagawa et al. 1996), or that ageing has no effect on most tendon mechanical properties (Hubbard & Soutas-Little, 1984; Johnson et al. 1994; Flahiff et al. 1995). An explanation for the above inconsistency may relate to interstudy differences between the population ages examined. For example, Shadwick (1990) and Nakagawa et al. (1996) included very young animals in their experiments, thus examining the effects of biological maturation and development, not the ageing process. From studies in which senile specimens have been included, however, it becomes clear that ageing makes the tendons more compliant, weaker and less rebound resilient than tendons from younger animals (Vogel, 1980, 1983; Blevins et al. 1994; Nakagawa et al. 1996). These changes are associated with: (1) an increase in non-reducible collagen cross-linking; (2) a reduction in collagen fibril crimp angle; (3) an increase in elastin content; (4) a reduction in extracellular water and mucopolysacharide content; and (5) an increase in type V collagen (Viidik, 1982; Tuite et al. 1997; Kjaer, 2004). Interestingly, factor 1 would stiffen a tendon; however, other factors, such as 2, 3 and 4, might bring about the opposite result. Clearly, differences in tensile phenomenological response between younger and older whole tendon specimens reflect the combined effect of all the above independent factors.
|
However, a method has recently been developed that allows examination of human tendon mechanical properties under in vivo conditions. The method is based on real-time ultrasound scanning of a reference point along the muscle–tendon unit during an isometric contraction of the in-series muscle. The muscle forces generated by contraction pull on the tendon and cause it to elongate (Fig. 4). The forces applied can be calculated from the external joint torque produced, the moment arm length of the muscle–tendon unit, and electromyographic activity measurements to quantify the effects of anatagonistic coactivation, if the contraction is generated by volition and not by stimulation. A number of versions of the above procedure have since been applied for the study of several human tendons and conditions (e.g. Maganaris & Paul, 1999; Kubo et al. 2001; Magnusson et al. 2001; Maganaris, 2002; Reeves et al. 2003a), but the effect of ageing has not been fully investigated.
|
15% than those of healthy older men (n= 6, 69–80 years of age). A study with a greater number of subjects and range of ages is imperative to further substantiate these preliminary findings. The ageing-related strength decline
A number of cross-sectional studies show that elderly individuals are considerably weaker than young adults (e.g. Hortobagyi et al. 1995; Roos et al. 1999; Macaluso et al. 2002). For example, in terms of knee extension and plantarflexion torque, older adults 70–80 years of age are 40% weaker than young adults 20–30 years of age (Roos et al. 1999; Klein et al. 2001; Macaluso et al. 2002; Morse et al. 2004). These reports are supported by findings from longitudinal studies, demonstrating a continual strength decline with ageing (Winegard et al. 1996; Lynch et al. 1999; Frontera et al. 2000), which is suggested to accelerate after the sixth decade of life (Narici et al. 1991).
The lower limbs experience greater ageing-induced reductions in strength compared to the upper limbs (Lynch et al. 1999; Frontera et al. 2000). Moreover, the extensor muscle strength at the knee and ankle appears to be more severely affected than the flexor muscle strength (Thelen et al. 1996; Winegard et al. 1996). This aspect of ageing demonstrates similarities with the response to short-term experimental unloading in healthy young adults, where the knee and ankle extensor muscles experience the greatest decline in strength and size (LeBlanc et al. 1988; Hather et al. 1992; Akima et al. 2001). These observations might indicate a greater loading requirement in order for the extensor muscle groups to maintain strength with ageing. Clearly the reductions in strength with ageing in the lower limbs are particularly relevant to locomotor activities. For example, knee extension power is closely related to walking speed in elderly individuals (Rantanen & Avela, 1997), and it is of concern that the ageing-related decline in power has been shown to parallel the reduction in maximal gait velocity (Kozakai et al. 2000). Although the causes of falls in the elderly are multifactorial, muscle weakness is believed to play a central role (Whipple et al. 1987; Feder et al. 2000; Khan et al. 2001; Skelton et al. 2002). The origin of this ageing-related strength decline involves muscular factors, such as changes at the single-fibre level (discussed above in the section on cellular and molecular determinants of sarcopenia), a decrease in whole-muscle specific tension (Morse et al. 2005c) and size; changes in tendon mechanical properties (discussed above in the section on tendon mechanical properties: fundamental concepts and the influence of ageing); neural mechanisms, such as a decrease in the number of active motor units due to collateral re-innervation (for reviews see Larsson, 1982; Roubenoff, 2001); and other hormonal and immunological factors (for review see Lamberts et al. 1997).
Strength gains with resistance training in old age
The progressive weakness experienced with ageing and the associated consequences for daily function clearly necessitate strategies to reverse, or at the very least to delay the progression of this process. In recent years, resistance exercise training has been shown to be an effective method for increasing strength in older adults (Frontera et al. 1988; Fiatarone et al. 1990; Roman et al. 1993; Welle et al. 1996; Hakkinen et al. 1998a,b, 2001; Harridge et al. 1999; Jozsi et al. 1999; Tracy et al. 1999; Scaglioni et al. 2002; Vincent et al. 2002a; Ferri et al. 2003; Reeves et al. 2004a,b, 2005b; Morse et al. 2005b). Typically the exercise training is performed using commercially available machines designed for one specific movement in a single plane. These resistance machines provide a constant external load that can be modified according to the desired training regimen. The training load is typically determined relative to a repetition maximum (RM), defined as the maximum load that can be lifted and lowered under control and repeated a given number of times. As it can be seen from Table 1A and B, which relates to resistance training programmes targeting the knee extensors in young and older adults, respectively, the training load can vary considerably between different studies, making conclusions on the relative effectiveness of a given exercise load very difficult to draw. This matter is further complicated by the different combinations of number of sets, number of training days per week and the total duration of the programme. Although it has been suggested that the training load should be between 60 and 100% of the 1RM in order to cause strength gains in the elderly (Evans, 1999), it may not be the load as a percentage of the repetition maximum that is the predominant factor. Clearly the load must be high enough to provide an effective mechanical stimulus that will induce adaptations; however, it may be that, as suggested for other musculoskeletal structures (Reeves et al. 2005a), the total volume of loading needs to exceed that experienced habitually by the system. Low-load resistance training at 50% of the 1RM has been shown to be effective for increasing strength in young adults only when combined with vascular occlusion to intensify the metabolic stimulus (Takarada et al. 2000, 2002). Training with the same load (50% of 1RM), but without vascular occlusion did not cause any significant changes in strength in young adults. Although these results may suggest that the training load needs to exceed 50% of the 1RM for older adults to increase strength, it must be considered that these findings relate to young adults, who are likely to experience greater habitual loads than older people and may therefore require higher relative training loads to increase strength. Indeed, this concept is supported by findings showing that relative increases in 1RM strength were similar between two groups of older adults training at either 50% of 1RM or 80% of 1RM (Vincent et al. 2002a).
|
Cellular and molecular adaptations to resistance training
Despite the loss of muscle mass, the decrease in motor unit number and the changes in myosin heavy chain composition, elderly muscle remains highly adaptable to training. Resistance training (6 months of high- and low-intensity weight training) has in fact been shown to reduce oxidative stress, thus potentially providing a protective effect against cellular ageing and sarcopenia (Vincent et al. 2002b). Resistance training has also been shown to reverse the fall in muscle protein turnover associated with ageing (Yarasheski et al. 1999; Dorrens & Rennie, 2003), probably by reducing the levels of tumour necrosis factor- (Greiwe et al. 2001), known to contribute to sarcopenia (Roubenoff et al. 2003).
At the single-fibre level, a reduction in the coexpression of multiple MHC isoforms (i.e. decreased distribution of hybrid fibres) has been found after 12 weeks of resistance training in elderly individuals (Williamson et al. 2000). Prior to resistance training, 31% of the total pool of muscle fibres was hybrid. After training, only 12% of the fibres coexpressed multiple isoforms, and the presence of pure MHC-1 fibres increased by 10%. Hence resistance training tends to oppose the age-associated increase in the coexpression of multiple MHC isoforms. This ‘protective’ effect of physical activity is also apparent in master athletes (Trappe, 2001). Older individuals who perform regular physical activity throughout their life tend to show a prevalence of pure MHC isoforms and a reduced expression of hybrid fibres (Klitgaard et al. 1990). However, these conclusions are in contrast to more recent findings of no changes in MHC isoforms after 12 weeks of training in older men, despite a 19% increase in maximum speed of sliding of (unregulated) actin on myosin (Vf), assessed by an in vitro motility assay (Canepari et al. 2005). This latter observation is particularly noteworthy because it showed for the first time that the function of the myosin molecule in old age can be modulated by exercise and that this effect may occur independently of changes in MHC isoforms. Also, since Vf measured by in vitro motility assay is not influenced by sarcomere geometry or by other myofibrillar proteins (troponins, titin or myosin binding protein C), the training-induced modulation of Vf is probably caused by a post-translational modification of myosin (Canepari et al. 2005) and is likely to determine the increase in unloaded shortening velocity (V0) reported by previous authors (Widrick et al. 1996; Trappe et al. 2000a,b). In contrast with the modulation of V0, no significant changes in specific tension of single fibres have yet been shown after strength training either in older men (Trappe et al. 2000b) or older women (Trappe et al. 2001). Nevertheless, because of the increase in V0, peak power of type I and IIa fibres normalized for cell cross-sectional area was, respectively, 2.3- and 1.6-fold higher after training in the older men (Trappe et al. 2000b) but, puzzling, not increased in the older women (Trappe et al. 2001). This apparent controversy may be related to the finding that V0 may not only be influenced by age but also by the training history of the individual.
Whilst it is important to develop an understanding of functional adaptations occurring at the molecular and cellular level with ageing and resistance training, whole-muscle function will not necessarily mimic these changes. In contrast to the situation in vitro, muscle is under voluntary control in the whole-body situation, and other musculoskeletal structures, such as tendon, are present, which will influence muscle–tendon unit function. Hence, a full understanding of the adaptations occurring with ageing and resistance training necessitates experiments performed in vivo at the level of the whole muscle–tendon unit.
Adaptations in the muscle–tendon unit with resistance training in old age
Muscular adaptations Although the strength gains with resistance training in old age are of primary importance, it is essential to develop an understanding of the adaptations occurring in the different motor system components. Muscular adaptations are central to any strength increase due to training and whilst it is widely believed that the degree of hypertrophy is directly proportional to the strength gains, this depends heavily upon how these two variables are measured and expressed (see sections entitled ‘Muscle architecture: fundamental concepts’ and ‘Influence of ageing on muscle architecture’). As mentioned above, the repetition maximum measured on the exercise device used for training is an inappropriate measure to describe the maximum force-producing potential of a muscle or muscle group. As shown by the force–velocity relation, higher forces can be developed during isometric contractions compared to those developed during any concentric contraction, and so this contraction type most closely represents the true force-producing potential of the muscle or muscle group.
In terms of quantifying the hypertrophic response to resistance training, ACSA measurements and the calculation of muscle volume from serial ACSAs along the muscle length have been reported. It has been shown from serial measurements of ACSA in various muscles for older adults that the largest increase in size occurs around the region of maximal muscle girth (typically the central region), with smaller increases or no changes towards the proximal and distal ends (Roman et al. 1993; Tracy et al. 1999; Reeves et al. 2004a). However, resistance training programmes in young adults lead to either uniform increases in ACSA throughout the muscle length (Higbie et al. 1996; Tesch et al. 2004) or non-uniform changes along the length (that are not largest around the maximal girth) that also vary for the constituent muscles of a muscle group (Narici et al. 1989, 1996b). The reason for the different distribution in ACSA changes along the muscle length with resistance training between young and older adults is not apparent, but it is likely to have implications for the valid assessment of training-induced hypertrophy. For example, a single ACSA measured in the mid-region of a muscle may overestimate the hypertrophic response following resistance training in older adults. Given this limitation, it could be suggested that muscle volume may more appropriately represent muscle hypertrophy due to training. However, an increase in both muscle ACSA and volume could theoretically occur owing solely to an increase in the number of sarcomeres in series. This implies that the above-mentioned methods of muscle size assessment cannot account for possible modifications to the internal muscle structure. A more accurate representation of the force-producing potential of a muscle and any possible changes with resistance training is given by the PCSA of the muscle, which takes into account both the internal spatial orientation and the length of muscle fascicles. Following a 14 week resistance training programme in older adults, we found that despite an average 6% increase in vastus lateralis muscle ACSA and volume, the PCSA of this muscle remained unchanged (Reeves et al. 2004a). Since the muscle PCSA remained unchanged and the estimated vastus lateralis muscle fascicle force increased by 11%, there was an increase in whole-muscle specific force (fascicle force/PCSA) of 19% after training (Reeves et al. 2004a).
Resistance training has been found to alter the internal muscle structure in older adults. Measured in the resting vastus lateralis muscle, fascicle lengths increased by 9% and pennation angles increased by 30% following resistance training in older adults (Reeves et al. 2004b). These training-induced adaptations in muscle architecture suggest increases in the number of sarcomeres in series and in parallel. An increase of sarcomeres in series has been shown in animal muscle in response to mechanical overload and stretch (Williams et al. 1988; Goldspink, 1998, 1999). It might be speculated that a greater number of in-series sarcomeres suggests that the muscle can operate across a wider range of lengths, but in vivo this is clearly limited by joint range of motion constrain. Nevertheless, the increased number of sarcomeres in series may influence the degree of sarcomere overlap, affecting the operating range of the muscle and subsequent force production. If all other conditions remain constant and it is assumed that the same absolute muscle length shortening occurs in pre- and post-situations, an increased number of in-series sarcomeres would cause a greater shortening of each sarcomere (Fig. 5). This theoretical effect would shift the operating range of the muscle to the left (towards shorter sarcomere lengths). As discussed above, however, the musculoskeletal system is remarkably plastic even in old age, and all other conditions may therefore not remain constant.
|
10 mm to longer lengths after resistance training, the estimated sarcomere operating range remained constant (Reeves et al. 2004b). The maintenance of the operating range of the muscle post-training is believed to reflect the interaction between changes occurring in muscle and tendon. Adaptations in these two musculoskeletal structures that exert opposing effects on sarcomere shortening may have interacted to cancel each other out and maintain the operating range of the muscle constant. It could be speculated that this is a natural strategy of the musculoskeletal system in order to maintain equilibrium with changes in the level of loading. The increase in stiffness of the patellar tendon in the above study occurred in the absence of tendon hypertrophy (Reeves et al. 2003a), which is consistent with findings in animals showing that tendons of mature animals adapt to increased levels of loading by increasing their material properties with no change in CSA (for review see Elliott, 1965). In addition to the implications for the operating range of the muscle discussed above, the training-induced increase in tendon stiffness will have implications for the speed of force transmission. Given the primary role of tendons as transmitters of contractile forces, an increase in tendon stiffness would be expected to make the tendon a more effective transmitting structure and increase the speed of force transmission. In line with this notion, from knee extension contractions performed as rapidly as possible, we observed an increase in the rate of torque development of 27% (Reeves et al. 2003a). This adaptation might be expected to increase the speed at which movements can be initiated.
|
The mechanical hysteresis of elderly patellar tendons has been shown to reduce from 33% before to 24% following resistance training (Reeves et al. 2003b; Fig. 6). Similar findings of reduced mechanical hysteresis have been reported in young adults after resistance training (Kubo et al. 2002). These results are in line with animal studies showing that tendons subjected to high physiological loads display lower mechanical hysteresis than tendons experiencing lower loads (Woo et al. 1980, 1981; Shadwick, 1990). In contrast to these results, no significant change in mechanical hysteresis was found after 6 months of low-load resistance training in middle-aged and older women (Kubo et al. 2003b). A reduction in mechanical hysteresis resulting from training may lead to metabolic energy savings during locomotor tasks. Although the energy returned upon tendon recoil may be increased, however, the total elastic energy recovered from the tendon will be dependent upon the total initial elongation, which was reduced by training (Reeves et al. 2003a). Any changes in tendon mechanical hysteresis induced by training might be most relevant for locomotion in the spring-like Achilles tendon.
In summary, structural and functional deterioration with ageing can be observed from the level of the single muscle fibre up to the whole muscle–tendon unit. However, many of the myotendinous factors characterizing ageing can be at least partly mitigated following resistance exercise training.
|
References |
|---|
|
TopAbstractReferences |
|---|
Ahtiainen JP, Pakarinen A, Alen M, Kraemer WJ & Hakkinen K (2005). Short vs. long rest period between the sets in hypertrophic resistance training: influence on muscle strength, size, and hormonal adaptations in trained men. J Strength Cond Res 19, 572–582.[CrossRef][Medline]
Akima H, Kubo K, Imai M, Kanehisa H, Suzuki Y et al. (2001). Inactivity and muscle: effect of resistance training during bed rest on muscle size in the lower limb. Acta Physiol Scand 172, 269–278.[CrossRef][Medline]
Alexander RM & Vernon A (1975). The dimensions of the knee and ankle muscles and the forces they exert. J Mov Stud 1, 115–123.
Alnaqeeb MA, Al Zaid NS & Goldspink G (1984). Connective tissue changes and physical properties of developing and ageing skeletal muscle. J Anat 139, 677–689.
Alnaqeeb MA & Goldspink G (1987). Changes in fibre type, number and diameter in developing and ageing skeletal muscle. J Anat 153, 31–45.[Medline]
Alway
SE, Degens
H, Krishnamurthy
G
&
Smith
CA (2002). Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am J Physiol Cell Physiol
283, C66–C76.
Andersen JL (2003). Muscle fibre type adaptation in the elderly human muscle. Scand J Med Sci Sports 13, 40–47.[CrossRef][Medline]
Andersen JL, Terzis G & Kryger A (1999). Increase in the degree of coexpression of myosin heavy chain isoforms in skeletal muscle fibers of the very old. Muscle Nerve 22, 449–454.[CrossRef][Medline]
Andersen
LL, Andersen
JL, Magnusson
SP, Suetta
C, Madsen
JL
et al. (2005). Changes in the human muscle force-velocity relationship in response to resistance training and subsequent detraining. J Appl Physiol
99, 87–94.
Blevins
FT, Hecker
AT, Bigler
GT, Boland
AL
&
Hayes
WC (1994). The effects of donor age and strain rate on the biomechanical properties of bone-patellar tendon-bone allografts. Am J Sports Med
22, 328–333.
Brooks
SV
&
Faulkner
JA (1988). Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol
404, 71–82.
Buchner DM, Cress ME, de Lateur BJ, Esselman PC, Margherita AJ et al. (1997). The effect of strength and endurance training on gait, balance, fall risk, and health services use in community-living older adults. J Gerontol A Biol Sci Med Sci 52, M218–M224.[Abstract]
Butler DL, Grood ES, Noyes FR & Zernicke RF (1978). Biomechanics of ligaments and tendons. Exerc Sport Sci Rev 6, 125–181.[Medline]
Canepari
M, Rossi
R, Pellegrino
MA, Orrell
RW, Cobbold
M
et al. (2005). Effects of resistance training on myosin function studied by the in vitro motility assay in young and older men. J Appl Physiol
98, 2390–2395.
D'Antona
G, Pellegrino
MA, Adami
R, Rossi
R, Carlizzi
CN, Canepari
M
et al. (2003). The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol
552, 499–511.
Delbono O (2000). Regulation of excitation contraction coupling by insulin-like growth factor-1 in aging skeletal muscle. J Nutr Health Aging 4, 162–164.[Medline]
Dirks AJ & Leeuwenburgh C (2005). The role of apoptosis in age-related skeletal muscle atrophy. Sports Med 35, 473–483.[CrossRef][Medline]
Dorrens J & Rennie MJ (2003). Effects of ageing and human whole body and muscle protein turnover. Scand J Med Sci Sports 13, 26–33.[CrossRef][Medline]
Elliott DH (1965). Structure and function of mammalian tendon. Biol Rev 40, 392–421.[Medline]
Evans WJ (1999). Exercise training guidelines for the elderly. Med Sci Sports Exerc 31, 12–17.[Medline]
Feder
G, Cryer
C, Donovan
S
&
Carter
Y (2000). Guidelines for the prevention of falls in people over 65. The Guidelines' Development Group. BMJ
321, 1007–1011.
Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J & Narici MV (2003). Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiol Scand 177, 69–78.[CrossRef][Medline]
Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA & Evans WJ (1990). High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263, 3029–3034.[Abstract]
Flahiff
CM, Brooks
AT, Hollis
JM, Vander Schilden
JL
&
Nicholas
RW (1995). Biomechanical analysis of patellar tendon allografts as a function of donor age. Am J Sports Med
23, 354–358.
Folland
JP, Irish
CS, Roberts
JC, Tarr
JE
&
Jones
DA (2002). Fatigue is not a necessary stimulus for strength gains during resistance training. Br J Sports Med
36, 370–373. [Discussion 374.]
Frontera
WR, Hughes
VA, Fielding
RA, Fiatarone
MA, Evans
WJ
&
Roubenoff
R (2000). Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol
88, 1321–1326.
Frontera
WR, Meredith
CN, O'Reilly
KP, Knuttgen
HG
&
Evans
WJ (1988). Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol
64, 1038–1044.
Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Day MK, Lee PL et al. (1992). Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. J Orthop Res 10, 928–934.[Medline]
Gadeberg
P, Andersen
H
&
Jakobsen
J (1999). Volume of ankle dorsiflexors and plantar flexors determined with stereological techniques. J Appl Physiol
86, 1670–1675.
Gans C & Bock WJ (1965). The functional significance of muscle architecture – a theoretical analysis. Ergeb Anat Entwicklungsgesch 38, 115–142.[Medline]
Garfinkel S & Cafarelli E (1992). Relative changes in maximal force, EMG, and muscle cross-sectional area after isometric training. Med Sci Sports Exerc 24, 1220–1227.[Medline]
Goldspink G (1998). Cellular and molecular aspects of muscle growth, adaptation and ageing. Gerontology 15, 35–43.
Goldspink G (1999). Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 194, 323–334.
Greiwe
JS, Cheng
B, Rubin
DC, Yarasheski
KE
&
Semenkovich
CF (2001). Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J
15, 475–482.
Hakkinen
K, Kallinen
M, Izquierdo
M, Jokelainen
K, Lassila
H, Malkia
E
et al. (1998a). Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol
84, 1341–1349.
Hakkinen K, Komi PV & Alen M (1985). Effect of explosive type strength training on isometric force- and relaxation-time, electromyographic and muscle fibre characteristics of leg extensor muscles. Acta Physiol Scand 125, 587–600.[Medline]
Hakkinen K, Kraemer WJ, Newton RU & Alen M (2001). Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiol Scand 171, 51–62.[CrossRef][Medline]
Hakkinen K, Newton RU, Gordon SE, McCormick M, Volek JS, Nindl BC et al. (1998b). Changes in muscle morphology, electromyographic activity, and force production characteristics during progressive strength training in young and older men. J Gerontol A Biol Sci Med Sci 53, B415–B423.[Abstract]
Harridge SD, Kryger A & Stensgaard A (1999). Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22, 831–839.[CrossRef][Medline]
Hather
BM, Adams
GR, Tesch
PA
&
Dudley
GA (1992). Skeletal muscle responses to lower limb suspension in humans. J Appl Physiol
72, 1493–1498.
Hebert
K (2004). Life expectancy in Great Britain rises – but later years are still spent in poor health. BMJ
329, 250.
Higbie
EJ, Cureton
KJ, Warren
GL
III
&
Prior
BM (1996). Effects of concentric and eccentric training on muscle strength, cross-sectional area, and neural activation. J Appl Physiol
81, 2173–2181.
Hook
P, Sriramoju
V
&
Larsson
L (2001). Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am J Physiol Cell Physiol
280, C782–C788.
Hortobagyi T, Zheng D, Weidner M, Lambert NJ, Westbrook S & Houmard JA (1995). The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. J Gerontol A Biol Sci Med Sci 50, B399–B406.[Abstract]
Hubbard RP & Soutas-Little RW (1984). Mechanical properties of human tendon and their age dependence. J Biomech Eng 106, 144–150.[Medline]
Ivey
FM, Roth
SM, Ferrell
RE, Tracy
BL, Lemmer
JT, Hurlbut
DE
et al. (2000). Effects of age, gender, and myostatin genotype on the hypertrophic response to heavy resistance strength training. J Gerontol A Biol Sci Med Sci
55, M641–M648.
Izquierdo
M, Hakkinen
K, Ibanez
J, Garrues
M, Anton
A, Zuniga
A
et al. (2001). Effects of strength training on muscle power and serum hormones in middle-aged and older men. J Appl Physiol
90, 1497–1507.
Johnson GA, Tramaglini DM, Levine RE, Ohno K, Choi NY & Woo SL (1994). Tensile and viscoelastic properties of human patellar tendon. J Orthop Res 12, 796–803.[CrossRef][Medline]
Jones
DA
&
Rutherford
OM (1987). Human muscle strength training: the effects of three different regimens and the nature of the resultant changes. J Physiol
391, 1–11.
Jozsi AC, Campbell WW, Joseph L, Davey SL & Evans WJ (1999). Changes in power with resistance training in older and younger men and women. J Gerontol A Biol Sci Med Sci 54, M591–M596.[Abstract]
Kawakami
Y, Abe
T
&
Fukunaga
T (1993). Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol
74, 2740–2744.
Kent-Braun
JA
&
Ng
AV (1999). Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol
87, 22–29.
Kent-Braun
JA, Ng
AV
&
Young
K (2000). Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol
88, 662–668.
Ker
RF (1981). Dynamic tensile properties of the plantaris tendon of sheep (Ovis aries).J Exp Biol
93, 283–302.
Khan
KM, Liu-Ambrose
T, Donaldson
MG
&
McKay
HA (2001). Physical activity to prevent falls in older people: time to intervene in high risk groups using falls as an outcome. Br J Sports Med
35, 144–145.
Kjaer
M (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev
84, 649–698.
Klein
CS, Rice
CL
&
Marsh
GD (2001). Normalized force, activation, and coactivation in the arm muscles of young and old men. J Appl Physiol
91, 1341–1349.
Klitgaard H, Mantoni M, Schiaffino S, Ausoni S, Gorza L, Laurent-Winter C et al. (1990). Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol Scand 140, 41–54.[Medline]
Knight CA & Kamen G (2001). Adaptations in muscular activation of the knee extensor muscles with strength training in young and older adults. J Electromyogr Kinesiol 11, 405–412.[CrossRef][Medline]
Kozakai R, Tsuzuku S, Yabe K, Ando F, Niino N & Shimokata H (2000). Age-related changes in gait velocity and leg extension power in middle-aged and elderly people. J Epidemiol 10, S77–S81.[Medline]
Kubo K, Akima H, Ushiyama J, Tabata I, Fukuoka H et al. (2004). Effects of resistance training during bed rest on the viscoelastic properties of tendon structures in the lower limb. Scand J Med Sci Sports 14, 296–302.[CrossRef][Medline]
Kubo K, Kanehisa H, Azuma K, Ishizu M, Kuno SY et al. (2003a). Muscle architectural characteristics in young and elderly men and women. Int J Sports Med 24, 125–130.[CrossRef][Medline]
Kubo
K, Kanehisa
H
&
Fukunaga
T (2002). Effects of resistance and stretching training programmes on the viscoelastic properties of human tendon structures in vivo. J Physiol
538, 219–226.
Kubo
K, Kanehisa
H, Kawakami
Y
&
Fukunaga
T (2001). Influence of static stretching on viscoelastic properties of human tendon structures in vivo. J Appl Physiol
90, 520–527.
Kubo K, Kanehisa H, Miyatani M, Tachi M & Fukunaga T (2003b). Effect of low-load resistance training on the tendon properties in middle-aged and elderly women. Acta Physiol Scand 178, 25–32.[CrossRef][Medline]
Lamberts
SW, van den Beld
AW
&
van der Lely
AJ (1997). The endocrinology of aging. Science
278, 419–424.
Larsson L (1982). Aging in mammalian skeletal muscle. In The Ageing Motor System, ed. Mortimer JA, Pirozzolo FJ & Maletta GJ, pp. 60–97. Praeger, New York.
Larsson L, Li X & Frontera WR (1997). Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 272, C638–C649.
LeBlanc
A, Gogia
P, Schneider
V, Krebs
J, Schonfeld
E
&
Evans
H (1988). Calf muscle area and strength changes after five weeks of horizontal bed rest. Am J Sports Med
16, 624–629.
Lexell J (1995). Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 50, 11–16.
Lexell J, Taylor CC & Sjostrom M (1988). What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84, 275–294.[CrossRef][Medline]
Lynch
NA, Metter
EJ, Lindle
RS, Fozard
JL, Tobin
JD, Roy
TA
et al. (1999). Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol
86, 188–194.
Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC & De Vito G (2002). Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25, 858–863.[CrossRef][Medline]
McMurdo
ME (2000). A healthy old age: realistic or futile goal?
BMJ
321, 1149–1151.
Maganaris CN (2001). In vivo tendon mechanical properties in young adults and healthy elderly. Proceedings of the Active Life Span Research Symposium. The Plasticity of the Motor System: Adaptations to Increased Use, Disuse and Ageing. Manchester Metropolitan University, UK.
Maganaris CN (2002). Tensile properties of in vivo human tendinous tissue. J Biomech 35, 1019–1027.[CrossRef][Medline]
Maganaris
CN, Baltzopoulos
V, Ball
D
&
Sargeant
AJ (2001). In vivo specific tension of human skeletal muscle. J Appl Physiol
90, 865–872.
Maganaris
CN
&
Paul
JP (1999). In vivo human tendon mechanical properties. J Physiol
521, 307–313.
Maganaris CN, Reeves ND, Rittweger J, Sargeant AJ, Jones DA et al. (2006). Adaptive response of human tendon to paralysis. Muscle Nerve 33, 85–92.[CrossRef][Medline]
, pennation angle; a, fibre cross-sectional area; PCSA, muscle physiological cross-sectional area; and T, muscle thickness. The two models have the same a, A and T. However, 
