Changes in morphology and function of ageing human skeletal muscle and the benefits of resistance training

(35 minute read)

The purpose of this literature review is to:

1. Investigate the age-related changes in human skeletal muscle morphology and function. Alterations in muscle volume, fibre area, fibre number and fibre composition changes, and the evidence of fibre type grouping and loss of functional motor units caused through a continuous neurogenic denervation/reinnervation process will be discussed. The deterioration in physical function and associated changes of reduced muscle strength, power and speed of muscle contraction, and questions concerning whether or not a loss of intrinsic muscle strength occurs with age, will be investigated. 
2. Explore the effects of resistance training in older adults and propose that instead of conceptualising the course of musculoskeletal decline as an immutable age-related process, changes in physical function across the lifespan can, in fact, be positively affected and potentially altered by physical activity and exercise. Resistance training will be recommended as such an activity that can provide significant benefits for the older individual by substantially improving muscle strength and power, eliciting muscle hypertrophy and enhancing functional mobility.

INTRODUCTION

Ageing is an inevitable consequence of all living creatures. Human beings are locomotive animals and contraction of muscular structures enable the skeletal system to move. Social expectations appear to support the decline of activity with advancing age (Ostrow and Dzewaltowski, 1986), thus making the age-related changes, a biopsychosocial phenomenon. Physical disuse will cause significant changes in human skeletal muscle structure and function (Lexell, 1993; Vandervoort and McComas, 1986). These alterations through disuse show a dramatic resemblance to age-related changes (Bortz, 1982). This prompts the suggestion that some of the deterioration evident in the neuromuscular system of the human, can be counteracted by appropriate levels of physical activity (Klitgaard, Marc, Brunet, Vandewalle and Monod, 1989a).  

With advancing age muscle volume declines, with a concomitant reduction in production of high muscle forces. This has been attributed to a continuous denervation/reinnervation process that causes a loss of functional motor units, due to the reinnervation capacity becoming so diminished that the fibres are consequently lost (Lexell, 1993). This process has been viewed as the major determinant of the decreasing muscle cross-sectional area with age. This loss of muscle mass appears to be the primary explanation of the significant reduction in strength (Rogers and Evans, 1993).

The intervention with resistance training or adherence to some form of resistive type exercise may have considerable effects on the ability of human skeletal muscle to maintain structure and function (Sipila and Suominen, 1993). Evidence strongly suggests that a progressive resistance training program may help improve the functional status of older individuals, with increments in strength and improvements in morphology (Fiatarone, Marks, Ryan, Meredith, Lipsitz and Evans, 1990). It is recommended that activity levels be maintained throughout the lifespan to ensure optimal functioning of the neuromuscular system, which will help sustain good quality of life and overall health.

MORPHOLOGICAL CHANGES IN AGEING SKELETAL MUSCLE

MUSCLE FIBRE TYPES

Human skeletal muscle can be divided into two different, but complementary fibre types which are based on their metabolic, ultrastructural, and physiological characteristics (Klitgaard, Mantoni, Schiaffino, Ausoni, Gorza, Laurent-Winter, Schnohr and Saltin, 1990; Komi, 1988; Rogers and Evans, 1993). Type I and II human skeletal muscle fibres vary significantly in their ability to generate force and also have differing fatigue indexes (Komi, 1988). Type I muscle fibres have a slow rate of force production, are fatigue resistant, have a low level of actomyosin adenosine triphosphatase (ATPase) activity, low glycolytic capacity, high mitochondrial density and therefore predominant during recruitment in aerobic activities of submaximal intensity (Komi, 1988; McArdle, Katch and Katch, 1986; Rogers and Evans, 1993). Conversely, type II fibres generate large amounts of force very rapidly, but are highly fatigable. This fibre type has been further sub-divided into type IIa and type IIb, with even suggestion of a type IIc muscle fibre (McArdle et al., 1986). The type IIa fibre is commonly referred to as the intermediate fibre of type I and type IIb (McArdle et al., 1986; Rogers and Evans, 1993), as it has a relatively fast rate of force production, but is also fatigue resistant (Komi, 1988). The type IIb fibre, in contrast, possesses the greatest anaerobic potential, with a large actomyosin ATPase activity, high peak and rate of force development and relatively low mitochondria (McArdle et al., 1986; Rogers and Evans, 1993). Research investigating human skeletal muscle morphology across the lifespan, most frequently report changes in fibre types I, IIa, and IIb.  

CHANGES IN MUSCLE FIBRE AREA AND FIBRE NUMBER

The volume of skeletal muscle is known to reduce with increasing age. However, whether this can be ascribed to ageing per se, or to other external factors, such as disuse (Bortz, 1982; Evans, 1992; Munnings, 1993) via decreasing activity levels, remains to be fully substantiated. Moreover, are the findings of Ostrow and colleagues (1981, 1986, 1987) which reveal that there are socially constructed levels of activity that are deemed appropriate to individuals of increasing age, and these beliefs and values are instilled in children as young as three years old. Evidently, the age-related changes that occur in human skeletal muscle are not just biologically influenced.

The observable decline in volume of ageing skeletal muscle can be explained through the findings of several investigations that demonstrate significant atrophy of type II muscle fibres, while the size of type I fibres remaining more or less unaffected (Clarkson, Kroll and Melchionda, 1981; Coggan, Spina, King, Rogers, Brown, Nemeth and Holloszy, 1992; Grimby et al., 1982; Larsson et al., 1979; Larsson et al., 1978; Larsson and Karlsson, 1978; Lexell and Taylor, 1991; Lexell et al., 1988; Oertel, 1986; Scelsi, Marchetti and Poggi, 1980; Stalberg, Borges, Ericsson, Essen-Gustavsson, Fawcett, Nordesjo, Nordgren and Uhlin, 1989; Trappe, Costill, Fink, Pearson and Vukovich, 1993). In addition to the decrease in size of type II fibres, there is also a progressive loss in number of muscle fibres, with both fibre types I and II being affected similarly (Lexell, 1992; Lexell et al., 1988). 

Fibre Area Changes- Type IIa versus Type IIb

Based on the selective atrophy of type II muscle fibres, it appears that the sub-types, IIa and IIb are affected dissimilarly with increasing age. In a longitudinal study conducted by Aniansson, Hedberg, Henning and Grimby (1986) no change in type I fibre area was observed over 7 years in 70 to 80 year old men, but type IIa and IIb fibre areas declined by 14 per cent and 25 per cent, respectively. In line with these findings were the results of Grimby et al. (1982) that showed (Figure 2: 130) decreases in type IIa fibre areas of 28.0 per cent and type IIb areas of 40.0 per cent, from approximately 20 to 80 years of age. The difference in the rates of decline with age between type IIa and type IIb fibre area illustrate the functional differences between these fibre types. This led Grimby et al. (1982) to suggest that these two subgroups should be separated in studies researching the relationship between function and morphology of human skeletal muscle. Other studies (Coggan et al., 1992; Klitgaard et al., 1990) have shown greater atrophy in older populations of type IIb muscle fibres as compared to type IIa fibres, implying that the age-related effects on human skeletal muscle morphology to be more extensive in type IIb fibres (Aoyagi and Shephard, 1992; Rogers and Evans, 1993). 

TOTAL NUMBER OF FIBRES

The reduction of muscle volume evident with increasing age may be mediated through not only a selective atrophy of type II muscle fibres, but also a change in the number of muscle fibres (Lexell and Downham, 1992). Work conducted by Lexell and colleagues (1988) demonstrated that the reduction in fibre size was moderate in comparison to the muscle volume reduction and therefore corresponded to the highly significant relationship found between the total number of fibres and muscle area. It was concluded that ageing atrophy seems to be caused by both a loss in fibre number (type I and type II equally affected) and decline of muscle fibre size (primarily type II fibres). At present, Lexell (1993) believes that the cross-sectional area (of the vastus lateralis muscle) is predominantly determined by the total number of fibres, and to a lesser extent by the size and/or the number of type II fibres. Hence, the current explanation for the decrease in muscle area with increasing age suggests that this is driven by an absolute loss of muscle fibres.

This position is supported by a recent project conducted by Klitgaard, Brunet, Maton, Lamaziere, Lesty and Monod (1989b) that assessed the influence of ageing and activity on the histochemical and metabolic characteristics of skeletal muscle in male wistar rats. The smaller muscle mass observed with ageing in the rats was initially attributed to an atrophy of fibre types followed by a marked hypoplasia or reduction in fibre number. There are difficulties though in extending these findings of animal studies to humans, yet such insights continue to remain a valuable tool to understanding the changing morphology of ageing human skeletal muscle. Additionally, there is the problem of the interpretation of results of studies using the muscle biopsy technique to assess age-related changes in muscle morphology due to the very small amount of muscle taken (Lexell, 1993; Lexell and Taylor, 1991; Rogers and Evans, 1993), and thereby suggests that the projects of Lexell and colleagues represent the most definitive data produced to date.

FIBRE TYPE DISTRIBUTION WITH AGEING

The effects of ageing on muscle fibre composition is contentious, although the extensive and recent cross-sectional projects conducted by Lexell and Downham (1992) and Lexell et al. (1988) support the position that the proportion of type II fibres remain unaffected by increasing age. However, most of the existing data has come from cross-sectional comparisons between different subgroups (Buskirk and Segal, 1989) and highlights the need for more longitudinal investigations.

Initial studies researching the effects of ageing on the distribution of type I and type II fibres reported a diminished proportion of type II muscle fibres and corresponding increase in type I muscle fibres. Larsson, Sjodin and Karlsson (1978) found that 20 to 29 year old insurance company clerks (n=11), of fairly low physical activity status had a distribution consisting of 40.5 per cent type I fibres in contrast to 55.0 per cent type I fibres in the 60 to 65 year old group (n=10). These results were further supported with later projects by Larsson, Grimby and Karlsson (1979), Larsson et al. (1978) and Scelsi, Marchetti and Poggi (1980) that showed a decrease in percentage type II fibre distribution. In the latter study, 45 nonwasted and noncachectic subjects aged 65 to 89 years of age were assessed and the 65 to 70 year old subjects had a 64.0 per cent expression of type I muscle fibres in comparison to the 81 to 89 year old group where 74.6 per cent of the muscle fibre population was comprised of type I fibres.    

The observation that a decreased percentage of type II fibres in human skeletal muscle is a result of the ageing process is further substantiated by a very recent study conducted by Trappe and co-workers (1993). The effects of ageing on muscle fibre composition in runners was examined after an 18-year period. Twenty male subjects (age= 51.6 +/- 3.1 years) had a muscle biopsy repeated on the gastrocnemius for histochemical analysis. The muscle samples taken in 1992 had significantly changed over the 18-year period, with the proportion of type I fibres increasing from 55.0 +/- 4.4 to 66.2 +/- 4.8 per cent. This longitudinal project provides much needed data on fibre compositional changes as a result of ageing. Nevertheless, extrapolation to all human muscles is problematic due to muscle assessment technique used.

Other investigations have produced data that is discordant, however, when compared to the abovementioned studies. These contend, to the contrary, that fibre type distribution does in fact remain unaltered (Clarkson, Kroll and Melchionda, 1981; Grimby, Danneskiold-Samsoe, Hvid and Saltin, 1982; Lexell and Downham, 1992; Lexell et al., 1988). Clarkson and colleagues (1981) found a coincident fibre type I percentage of 40.7 for their young subjects when compared to Larsson et al. (1978) value of 40.5 per cent for their 20 to 29-year-old group. However, muscle fibre type composition did not change in favour of type I in Clarkson et al. (1981) study, when young and old groups were compared. This finding was supported by Grimby et al. (1982) who found that muscle fibre composition in 78 to 81-year-old men and women did not differ between either gender or the younger sedentary subjects.

At present, most studies that have evaluated the ageing process on muscle fibre composition have used the muscle biopsy technique. Consequently, only a very small percentage of whole human muscles can be analysed, which thereby limits our knowledge of the composition of individual human muscles at different ages and the variability between individuals (Lexell, 1993; Lexell and Taylor, 1991). However, Lexell and associates (1986, 1988, 1991, 1992) have been able to prepare and analyse cross-sections of whole human muscles from autopsies and have thus overcome the problems inherent in muscle biopsy techniques.

The results from Lexell, Downham and Sjostrom’s (1986) investigation showed that muscle fibre composition did not alter significantly between the ages of 15 and 83 years in men. The proportion of type I fibres was 49 +/- 5 per cent compared to 51 +/- 9 per cent, respectively. It therefore appears that individual human muscle retains its proportion of fibre types from the second decade up to and including the eighth decade of life. Nonetheless, establishing clarity regarding muscle fibre composition changes with ageing is difficult due to the shortcomings of both cross-sectional and muscle biopsy research. Therefore, it remains open to debate as to whether or not muscle fibre composition alters toward an increased expression of type I fibres. 

FIBRE NUMBER LOSS, DENERVATION AND REINNERVATION

The progressive loss of both muscle fibre types can be caused by either damage to the fibres, which are then unable to be repaired and regenerated, or a permanent loss of contact between the nerves and the muscle fibres (Rogers and Evans, 1993; Lexell et al., 1988). Myopathic changes in ‘normal’ ageing skeletal muscle are rarely seen, whereas extensive neuropathic changes are quite common (Grimby et al., 1982; Lexell et al., 1988). Increased fibre type grouping (Grimby et al., 1982; Lexell et al., 1986; Scelsi et al., 1980), loss of functional motor units (Brown, Strong and Snow, 1988; Stalberg et al., 1989; Vandervoort and McComas, 1986) and degeneration of the end plate complex (Wokke, Jennekens, van den Oord, Veldman, Smit and Leppink, 1990) have all been seen as evidence of a continuous denervation and reinnervation process, whereby some motoneurons increase their own motor unit area (Oertel, 1986; Vandervoort, 1992). This age-related progressive neurogenic process may begin before 50 years of age and must be a major factor in the loss of muscle fibres with increasing age (Lexell et al., 1986).  

Fibre Type Grouping and Enclosed Fibres

Several projects (Grimby et al., 1982; Lexell et al., 1986; Oertel, 1986) have investigated the fibre type arrangement in muscles at various ages, and an incremental occurrence of fibre type grouping – assessed as the number of enclosed fibres [a fibre surrounded entirely by fibres with the same histochemical properties (Lexell et al., 1986)] – was noticed in older individuals. In the study conducted by Lexell and associates (1986), the old group (men between 71 to 83 years of age), had a significantly higher proportion of enclosed fibres (21 per cent), than the proportion for the middle group, aged 49 to 56 years of age (6 per cent), and the young group, aged 15 to 35 years of age (6 per cent). It was concluded that fibre type arrangement was segregated and ungrouped in young muscles of 25 years and less. From 30 to 60 years of age, the arrangement of fibre types was random, in contrast to age 60 and above where an excess of enclosed fibre type grouping was evident. Fibre type grouping therefore seems to be a normal part of the ageing process in old muscle.  

This process of fibre type grouping has recently been noticed to not only affect the m. vastus lateralis (Aniansson, Zetterberg, Hedberg and Henriksson, 1984; Lexell et al., 1988; Lexell et al., 1986), but additionally, the deltoid muscle as recognised by Oertel (1986). This study also analysed the frequently biopsied vastus lateralis muscle for comparisons with previously reported data. Results indicated that small and large fibre type groupings were age-related, with fibre type grouping in small groups predominating in autopsy specimens up to 40 years of age.  Conversely, large groups of fibre type grouping were demonstrated in cases over 60 years of age. The earlier investigation by Scelsi et al. (1980) confirmed the large fibre type grouping occurs at an accelerating rate after 70 years of age. His findings displayed extensive grouping of fibres in the m. vastus lateralis in 45 healthy sedentary men and women between 65 and 89 years of age. There was a dramatic increase in significant fibre type grouping from the age group 65 to 70 years of age (5 per cent of cases) as compared to the 81 to 89-year-old group (60 per cent of cases).

The results of Grimby et al. (1982) concur with these findings where fibre type grouping and enclosed fibres were more prevalent in subjects of 70 years and older. Interestingly, however, was the significant and exclusive grouping and enclosure of type I fibres in the m. vastus lateralis of the elderly 78 to 81-year-old men and women. This differed from the biopsy samples taken from the bicep brachii, which showed far fewer enclosed fibres and groupings. When comparing Oertel’s (1986) and Grimby et al. (1982) studies, discrepancies appear with respect to fibre type grouping in upper and lower extremities. The former study found a similar degree of fibre type grouping in lower and upper body segments, in contrast to the latter study that found significant differences between the amount and degree of fibre grouping in lower and upper segments. These discordant findings may be related to the different techniques used (autopsy versus muscle biopsy) to assess the microscopic morphological alterations in ageing muscle, and the specific variation in the muscle groups (m. vastus lateralis, deltoid and biceps brachii) studied.

Motor Unit Loss

Research exploring the phenomenon of motor unit losses supports the hypothesis that there is an ongoing denervation and reinnervation of the motoneuron pool, and this produces an increase in motor unit areas (Brown et al., 1988; Stalberg et al., 1989; Vandervoort and McComas, 1986). Brown and associates (1988) established that there was a decline in the number of motor units in the biceps-brachialis muscles, especially in the older subjects. Estimations suggest that the complement of motor units in subjects in the third decade had declined to about half in subjects over 60 years of age. This represents a loss of about 10 to 20 motor units per year, or approximately one per cent of the total per year (Brown et al., 1988).

The motor unit number decrement in 65 clinically healthy subjects, aged 20-70 years (31 females and 34 males) was also assessed in the m. vastus lateralis by Stalberg et al. (1989) through electrophysiological methods. The fibre density parameter was calculated from 20 recording sites and was taken as being indicative of the average number of muscle fibres per motor unit. A technique called macro EMG amplitude was used coincidently with the fibre density parameter and was representative of the overall size of the motor unit(s) complex. Results demonstrated that fibre density increased linearly with age in both sexes, with an approximate 56 percent difference between 20 and 70-year-old subjects. This increase in fibre density implies that motor unit reorganization via a denervation/reinnervation process occurs with age. The concomitant increases in macro EMG amplitude of 27 to 36 per cent in age groups of 60 to 70 years, compared with 20 to 50-year olds, indicated that there had been an overall increase in motor unit size. Vandervoort and McComas (1986) found a reduction of functioning motor units in the soleus muscle of approximately 70 per cent in men and women between 80 to 100 years of age, after comparison with the young and middle-aged adults. This is consistent with previous studies that have displayed a tendency for the remaining motor units to become progressively larger (Rogers and Evans, 1993). This alteration in motor unit size has been viewed by Stalberg and co-workers (1989) as a compensatory process due to the loss of motor units with age. 

Taken together, these results demonstrate that the muscle fibre population is continuously undergoing a denervation and reinnervation process with advancing age. This accelerating loss of functioning motor units appears to begin around 50 years of age (Lexell, 1993). The loss of muscle fibres, and muscle volume can therefore be attributed largely to this alteration and loss of the motor unit pool with advancing age (Lexell et al., 1986).

CHANGES IN MUSCLE FUNCTION

CHANGES IN MUSCLE CROSS-SECTIONAL AREA AND STRENGTH

The linear relationship that exists between muscle cross-sectional area and strength is well acknowledged (Aoyagi and Shephard, 1992; McArdle et al., 1986). With increasing age there is an accelerating and progressive reduction in muscle volume as determined by cross-sections of whole human muscles (Lexell et al., 1988), various radiological techniques (Greig, Botella and Young, 1993; Overend, Cunningham, Kramer, Lefcoe and Paterson, 1992; Rice, Cunningham, Paterson and Lefcoe, 1989; Sipila and Suominen, 1993; Sipila and Suominen, 1991; Vandervoort and McComas, 1986; Young, Stokes and Crowe, 1984), hydrostatic weighing techniques (Frontera, Hughes, Lutz and Evans, 1991), creatinine excretion determination (Frontera et al., 1991; Kallman, Plato and Tobin, 1990) and less specific anthropometric measurements (Bassey, Fiatarone, O’Neill, Kelly, Evans and Lipsitz, 1992; Kallman et al., 1990; Larsson et al., 1979; Rice, Cunningham, Paterson and Rechnitzer, 1989). This reduction in muscle volume with increasing age correlates closely to the observable decline in muscle strength (Kallman et al., 1990; Overend et al., 1992; Sipila and Suominen, 1991). The quantitative loss of contractile protein, mainly attributed to a loss of muscle fibres due to muscular and/or neural alterations (Lexell et al., 1988) in addition to a selective atrophy of type II fibres (Grimby et al., 1982; Lexell and Downham, 1991) is but one explanation for the decline of strength with increasing age. Other potential factors include a decrease in the ability of skeletal muscle to generate tension due to localized changes (for example, a change in fibre length or angle), a reduced capacity of the central nervous system to activate motor units, or a combination of all these mechanisms (Frontera et al., 1991).

The projects of Lexell et al. (1988) and Rice et al. (1989a) clearly demonstrate that muscle volume declines with age. Lexell et al. (1988) reported that reduction of the m. vastus lateralis muscle begins as early as 25 years of age, and that by age 50 approximately 10 percent of the muscle area is lost. This was determined through cross-sections of whole human muscles from autopsies performed on previously healthy 15- to 83-year-old males. Assessment of muscle volume from age 50 to 80 years of age indicate that there is an accelerated reduction with close to half of the muscle area wasted. 

The computed tomography scans that were taken by Rice et al. (1989a) demonstrated that total cross-sectional area of the elderly (65-90 years of age) arm flexors and extensors were 31 and 25 per cent smaller, respectively, than the young subjects (25-38 years of age). In contrast, the plantar flexor cross-sectional area of the elderly was only 22 per cent smaller. However, when comparisons were made between the elderly and young groups, non-muscle tissue components of the arm flexors, extensors and plantar flexors were considerably higher (27%, 45% and 81%, respectively). The net effect of these findings demonstrated a similar decline in contractile tissue of the elbow flexors (36 per cent), elbow extensors (28 per cent) and plantar flexors (35 per cent). The authors concluded that an accelerated infiltration of non-muscle tissue may occur in the plantar flexors beyond after 70-75 years of age.

Young, Stokes and Crowe (1984) studied the cross-sectional area and strength of the quadriceps muscles through compound ultrasound imaging and isometric strength assessment, in old (71-81 years) and young (20-29 years) women. The results indicated that the older women were 35 per cent weaker than the young women and their quadriceps cross-sectional area was 33 per cent less. Conversely, Larsson and associates (1979) observed that, between 20 and 69 years of age, men showed a decline in isometric quadriceps strength, but no change in thigh circumference as determined anthropometrically. However, alterations in body composition toward increasing connective tissue and inter- and intra-muscular adipose deposits may account for the indiscernible changes in cross-sectional area when determined anthropometrically (Sipila and Suominen, 1993).

Bassey and associates (1992) contend however, that power is more sensitive to age-related losses than strength, and is therefore a more relevant measurement. Consequently, the assessment of leg extensor power of 13 men, (mean age= 88 +/- 1.6 years) and 13 women (mean age= 86 +/- 1.5 years) was undertaken. This enabled a comparison to be made with previous data on non-athletic young adults (Bassey and Short, 1990). The results showed that the elderly subjects had about 20 per cent of the muscle power found in non-athletic young adults (Bassey and Short, 1990). In comparison, there is much greater power loss with age versus strength loss (Greig et al., 1993; Rice et al., 1989b; Young et al., 1984). This difference was ascribed to the recruitment patterns of the muscle power and muscle strength being somewhat dissimilar. The speed component of power increases the dependency on recruitment of type II fibres and this is consistent with the findings that these fibres are selectively atrophied with age (Lexell et al., 1988; Trappe et al., 1993). 

Another recent cross-sectional study (Frontera et al., 1991) assessed the isokinetic strength of the elbow (60 and 180 degrees per second) and knee (60 and 240 degrees per second) extensors and flexors in 200 healthy 45 to 78-year-old men and women. In addition, body composition determinations were estimated via hydrostatic weighing, for fat-free mass, and creatinine excretion (representative of muscle mass). Muscle mass determinations were based on work conducted by Heymsfield, Arteaga, McManus, Smith and Moffit (1983) that estimated the equivalence of 18.5 kilograms of muscle for every gram of urinary creatinine.

The results indicated that absolute isokinetic strength of the knee extensors and flexors was 20.0 and 22.0 per cent lower in elderly men, and 17.6 and 15.5 per cent lower in elderly women than the younger groups of the same gender, respectively. For the elbow extensors and flexors isokinetic strength was 20.0 and 20.8 per cent lower in older men, and 22.2 and 16.7 per cent lower in older women. Such age-related strength losses imply that both upper and lower segments decrease at a similar rate. Interestingly, when strength was adjusted for fat-free mass, the age-related differences were only statistically significant for knee extensor torque when tested isokinetically at 240 degrees per second. This suggests that strength loss with age can be primarily be attributed to the loss of muscle mass, whereas the loss of power when performing high speed leg extension movement is due to both the loss of muscle mass and neurological deficits  onetheless, it was suggested that a differential loss of strength occurred between the upper and lower extremity muscles, with a faster decline in the strength of the knee extensors and knee flexors, than in the elbow extensors and elbow flexors muscle groups with advancing age (Shelley, Snow-Harter, Robinson, Wegner and Shaw, 1993). This incongruity with the data, does however, place doubts on the validity of whether differing rates of strength losses do actually occur between upper and lower limbs with advancing age. Reasons for this possible variation between upper and lower extremities, can be ascribed to a possible decreasing use of lower limb muscles and paralleling drop in forceful contractions, as compared to upper limb muscles, thus contributing to the type II fibre atrophy known to occur with age (Grimby et al., 1982; Lexell et al., 1988; Trappe et al., 1993).

Very few longitudinal studies have investigated the loss of muscle strength and/or muscle cross-sectional area with age. Aniansson et al. (1986) found that quadriceps muscle strength decreased by 10 to 22 per cent at five different contraction velocities in 23 men aged 73-83 years over a 7-year period. This contrasted to a small reduction in body weight (2 per cent) and total body cell mass (6 per cent). This strongly highlights the need to discriminate between muscle tissue and non-muscle tissue components, so that the relative contribution of the loss of muscle tissue to the observed decline in muscle strength with age can be established.

Kallman and associates (1990) studied the effects of ageing on grip strength from a longitudinal and cross-sectional perspective. Grip strength and muscle mass (as estimated by creatinine excretion and forearm circumference) were measured in 847 healthy subjects, aged 20-100 years, from the Baltimore Longitudinal Study of Ageing. Both perspectives concur that grip strength increases into the fourth decade of life and declines from thereon at an accelerating rate. What is of interest, however, is the findings that show not all subjects lose grip strength as they age. Subjects less than 40 years of age, 40-59 years of age and older than 60 years, showed no observable decline amounting to 48, 29, and 15 per cent, respectively, in grip strength during the 9-year average period of the study. Furthermore, results indicated through comparisons of actual strength to strength predicted by forearm girth or creatinine excretion, that subjects up until 55 years of age are stronger than predicted. After this, older subjects are weaker than predicted, with the difference between actual and estimated strength, increasing in the older age groups.

Kallman et al. (1990) also conducted a regression analysis of individual rates of change of grip strength on rates of change of muscle mass, as estimated by creatinine excretion, and found that there was no relationship between how fast subjects lost muscle mass and how fast they lost grip strength. This strongly suggests the decline in grip strength with increasing age requires other explanations beyond declining muscle mass. The authors consequently viewed alterations in muscle fibre composition and motoneuron abnormalities [denervation/reinnervation process whereby the larger motor units become less efficient (Lexell et al. (1993)] as possible age-related changes contributing to the study’s results.

Very recently Greig and co-workers (1993) produced data that was incongruous with Kallman et al. (1990) study after retesting the quadriceps strength of 14 healthy elderly subjects (ranging in age from 79-89 years) from an original study conducted 8 years previously that consisted of 37 healthy women and men. The difficulties of longitudinal studies become clearly apparent with only 14 subjects able to be traced for the follow-up study. Nevertheless, comparisons made in respect to the original findings were seen as highly valid and reliable. Lifestyle patterns over the intervening years had remained similar, with activity patterns, in particular, demonstrating no significant alterations. It should be emphasised that the data reported from this project is unique. Presently, there does not appear to be any longitudinal research relating specifically to leg extensor strength in people 79-89 years of age.

Following a comparison of the data collected for this investigation, statistical analysis demonstrated no significant evidence for any loss of isometric quadriceps strength at all (95 per cent confidence interval: loss of 1.4 % to gain of 0.8 % per annum). This lack of strength loss appears astounding, given the advanced age of these subjects. Cross-sectional studies consistently suggest that muscle strength peaks in the third decade, followed by relatively well maintained levels up until approximately 50 years of age, declining at about 15 per cent per decade in the sixth and seventh decade, and accelerating to 30 per cent per decade thereafter (Buskirk and Segal, 1989; Danneskiold-Samsoe et al., 1984; Frontera et al., 1991; Kallman et al., 1990; Larsson and Karlsson, 1978 (Fig 1): 132; Rogers and Evans, 1993; Stalberg et al., 1989). This cross-sectional data implies that strength losses should be clearly evident and significant in the eighth and ninth decades of life. On the contrary, however, was the lack of change in strength of the subjects involved in Greig et al. (1993) study. In addition and most importantly are the implications from this (first) longitudinal study which confirm some authors opinions (Bortz, 1982; Lexell and Taylor, 1991), which have suggested quite clearly that physical inactivity may play a highly significant role in the age-related muscle function alterations.

With the maintenance of strength levels in Greig et al. (1993) study, it was postulated that the high levels of habitual physical activity led to an attenuation in the decline of muscle strength. Furthermore, it was speculated that an unusual slow rate of loss of strength is “a favourable ‘risk factor’ for ‘successful ageing’ explaining the predominance of this feature amongst our subjects” (1993: 10). Perhaps the only disappointing aspect of this study, however, was the assessment of the cross-sectional area of the quadriceps muscle, which was done originally with ultrasonography and repeated with CT scanning in the follow-up study (ultrasonography was not available). Although ultrasonography is highly correlated with CT scanning, the latter is reported to yield on average, 30 per cent larger cross-sectional areas (Sipila and Suominen, 1993). For this reason, the results of Greig et al. (1993), that indicated a 0.8 per cent decrease in cross-sectional area per annum, should be interpreted with caution. It seems possible, in the authors opinion that the change from ultrasonography to computed tomography may have concealed some of the reduction in cross-sectional area. This would therefore imply that other factors are influencing the maintenance of strength, apart from cross-sectional area. This can be clarified when it is acknowledged that strength levels remained statistically similar, while concomitantly, cross-sectional area appeared to decrease.

The results of the abovementioned investigation calls into question the conclusions of many cross-sectional studies cited above. Furthermore, the data presented by Aniansson et al. (1986), which emerged from a longitudinal analysis, is in direct opposition to the recent findings of Greig et al. (1993). Nevertheless, the discrepancy between these two investigations has been attributed to the contrasting levels of habitual activity, with the subjects of the former study seemingly far less habitually active than the subjects of the latter study. Many factors, such as levels of physical activity, nutritional status, disease status, and mental attitude (Buskirk and Segal, 1989) exacerbate the difficulty of producing valid, reliable and representative data for the age-related changes in morphology and function of human skeletal muscle, from both longitudinal and cross-sectional perspectives. Hence, the establishment of concordance on whether the age-related changes are due primarily to ageing per se, or perhaps on the other hand, disuse, remain open to debate. 

INTRINSIC MUSCLE STRENGTH- Problems with determining maximal voluntary force to cross-sectional area (MVF/CSA)

The assessment of the ratio of maximal voluntary force to muscle cross-sectional area (MVF/CSA) has been investigated in several projects (Frontera et al., 1991; Kallman et al., 1990; Overend et al., 1992; Phillips, Bruce, Newton and Woledge, 1992; Vandervoort and McComas, 1986; Young et al., 1984) in an attempt to establish whether losses of muscle strength are partially due to human skeletal muscle becoming intrinsically weaker with increasing age. The difficulty, however, of accurately determining this parameter are well acknowledged (Frontera et al., 1991; Phillips et al., 1992; Sipila and Suominen, 1993) as there are a multitude of factors and many confounding variables, which thereby produce spurious data, results, and therefore conclusions.

Accurate determination of MVC/CSA depends on precise measurement of both factors in the ratio (Overend et al., 1992). The variability in the constituencies (that is, muscle and non-muscle components) of elderly and young cross-sectional areas, incorporates a considerable chance of making incorrect comparisons once MVC/CSA is ascertained. Of relevance here in the denervation/reinnervation process which has been extensively addressed by Lexell and associates (1988). Having established earlier that the muscle fibre population undergoes continuous denervation and reinnervation with increasing age (most likely caused through an accelerating loss of functioning motor units), a phase will be reached where the reinnervation capacity is so compromised that the muscle fibres are permanently denervated and correspondingly, lost. Subsequently, this loss of contractile tissue is replaced by adipose and fibrous tissue. Estimations indicate that for younger individuals (15-35 years) approximately 70 per cent of the muscle area is comprised of muscle fibres. The elderly (70-80+ years) muscle CSA on the other hand, shows a disparate constitution of muscle fibres when compared to younger muscle CSA. Estimations in this age bracket, predict approximately 50 per cent of muscle CSA is composed of muscle fibres and the other 50 per cent is adipose and connective tissue. This is in line with other studies (Rice at al., 1989a; Sipila and Suominen, 1991; Young et al., 1984) that have shown increasing amounts of intra-muscular connective tissue and infiltration of fat deposits into lean tissue, with advancing age. In light of these findings it is clear that an overestimation of effective cross-sectional area could result through indefinitive measurements, which would thereupon underestimate the MVF/CSA.

Additionally, Phillips and associates (1992) have recognised that the fibre type arrangement will also influence MVF/CSA. Studies investigating muscle groups with complex pennate fibre arrangements (for example, the quadriceps femoris group), should realise that the cross-sectional area of the muscle will not be the same as the summated cross-sectional area of all the fibres. The interaction between this observation and the aforementioned findings of Lexell et al. (1988) may further complicate the accurate assessment of MVF/CSA in young and old subjects.

Presently, there is evidence which has demonstrated the considerable error associated with in vivo techniques when calculating cross-sectional areas. Sipila and Suominen (1993) found, as mentioned previously, that computed tomography produced 30 per cent larger cross-sectional areas than ultrasonography. This difference was partly due to the thick connective tissue fasciae surrounding different muscles and groups of muscles. These components were discernible and therefore left out from the cross-sectional areas when using ultrasonography, in contrast to computed tomography where they had to be included as they were indiscernible. Another problem included the incapacious ability of both techniques to clearly indicate the medial border of the vastus medialis. All of the abovementioned problems pose serious questions about the validity of the findings to date related to MVF/CSA as presented below.

INTRINSIC MUSCLE STRENGTH (MVF/CSA) – Does it decline with increasing age?

The decline of strength with increasing age is a multifactorial phenomenon, that is perhaps caused by a combination of declining muscle mass and alterations in muscle contractility (Rogers and Evans, 1993). There is evidence to suggest that the reduction of strength may be greater than the absolute loss of muscle mass (Kallman et al., 1990; Overend et al., 1992). Vandervoort and McComas (1986) found that the decline in the cross-sectional areas of the gastrocnemius and soleus muscles with age (20-100 years of age) could not account for the absolute decrease in voluntary plantarflexor strength. This suggested that the capacity to generate force per unit of cross-sectional area had been affected in the older subjects. Nonetheless, these authors believed that the decrease was probably due, in part, toward an increase representation of non-contractile tissue in the cross-sectional area.

Overend and co-workers (1992) assessed the relationship between isometric and isokinetic-concentric knee extensor and flexor strength, and quadriceps and hamstring cross-sectional area in 13 young (age 19-34) and 12 elderly (age 65-77) men. The results were inconclusive in relation to whether MVF/CSA decreased or remained similar with advancing age. Absolute isometric strength in the elderly men decreased significantly from the younger subjects, however, this could be explained by the smaller cross-sectional areas. In contrast, the decrease in isokinetic-concentric strength was greater than could be accounted for by the decrease in muscle cross-sectional area. In another study conducted Cunningham, Morrison, Rice and Cooke (1987) isokinetic torques at 30, 60, 90, 120 and 180 degrees per second were assessed in young (21.7 +/- 2.0 years) and older (63.3 +/- 2.8 years) men. It was shown that age was a significant factor of plantar flexion torque at 180 degrees per second, but not at all at the lower velocity of 30 degrees per second. Both of these projects were completed at the same laboratory, and the cause of the observable decrements in MVF/CSA and torque values were ascribed, in part, to the preferential atrophy of type II fibres in elderly men.

The dissimilarity between the cross-sectional area of a complex pennate muscle (for example, vastus lateralis) and the summated cross-sectional area of all the fibres in that muscle, has the influence of causing relatively weak correlations between MVF and cross-sectional area. This led Phillips and associates (1992) to investigate one of the mechanisms (that is, activation) by which MVF/CSA is reduced in the adductor pollicis due to its’ almost parallel fibred arrangement. Consequently, there is a very strong correlation between MVF and cross-sectional area.

The data produced a 26 +/- 3 % less MVF in the elderly than that predicted from their cross-sectional area using the regression line for the young subjects. Yet, an important possible source of muscular weakness was dispelled through the utilization of the twitch interpolation technique, that showed even the elderly subjects with a reduced MVF/CSA were capable of full activation during a maximal voluntary contraction. Another confounding variable which complicates the interpretation of Phillips et al. (1992) project, has been discussed by Belanger and McComas (1981), where it was acknowledged that other muscles, in addition to the adductor pollicis, can contribute to the adduction of the thumb. Furthermore, complete elimination of the action of these muscles is difficult to achieve, which thereby produces an overestimated MVF for the adductor pollicis muscle. These variables and the possibility that the synchronization ability of older subjects may be compromised compared to younger subjects (Sale, 1988), coupled with other muscles influencing the adductor pollicis MVF, may create a disproportionate level of strength expression in the younger subjects and therefore MVF/CSA.

The measurement of the cross-sectional area of the adductor pollicis muscle by Phillips et al. (1992) was determined via differences in outputs from two linear potentiometers which were moved over the skin, and this has been shown to be well correlated to computed tomography. Nonetheless, with the possibility of an increasing infiltration of non-muscle tissue with advancing age (Lexell et al., 1988; Rice et al., 1989a), the problematic nature of the computed tomography (CT) technique (Silipa and Suominen, 1993) and the fact that the technique used by Phillips et al. (1992) was not as definitive as the CT scanning technique, throws doubt upon whether the MVF/CSA parameter was accurate.

The problems inherent in determining accurate cross-sectional areas through radiological techniques was avoided by Frontera et al. (1991) through hydrostatic weighing (estimation of fat-free mass) and creatinine excretion (estimation of muscle mass) techniques. This study has been addressed above and therefore only the data relating to MVF per kilogram of muscle mass will be mentioned here. Decreases in absolute strength of the knee extensors and flexors, and elbow extensors and flexors, were observed in the elderly men when compared to the younger men. However, and most notable, was the finding that these strength losses when corrected for fat-free mass and muscle mass were significantly reduced and/or completely eliminated, hence producing non-significant age-related differences, which were independent of the muscle group and movement. The authors concluded that the strength differences were most likely caused by alterations in muscle mass and not by impaired muscle function.

This conclusion was supported by Young et al. (1984) which showed MVF (isometric) of the quadriceps and cross-sectional area of older women (age 71-81) to be 35 and 33 per cent lower, respectively, than the younger women (age 20-29). These results once translated into MVF/CSA, showed no difference between the young and old women. This suggests that there was no change in the intrinsic strength of the quadriceps femoris muscle in the older women, as compared to the younger women, and supports the contention that the loss of strength with advancing age is predominantly caused through a loss of functioning muscle mass.

The many problems associated in attempting to accurately determine the MVF/CSA parameter have been outlined above. As a result, conflicting reports have continually been produced in the literature and have therefore maintained the highly disputable status of this parameter. In consideration of the evidence relating to MVF, cross-sectional area and MVF/CSA, it would appear that much of the decline in muscle strength is accounted for by a reduction in muscle cross-sectional area, rather than ageing skeletal muscle becoming intrinsically weaker (Grimby et al., 1982; Frontera et al., 1991; Lexell and Downham, 1992; Lexell et al., 1988; Rogers and Evans, 1993: Young et al., 1984). More research is required although, due to the large variability in opinions which are evident in the literature.

MUSCLE CONTRACTILE PROPERTIES

Studies of electrically evoked human muscle strength as a function of age are limited (Vandervoort and McComas, 1986), however, ageing seems to prolong the twitch contraction, half-relaxation times and contraction time to tetanus, while concomitantly reducing twitch potentiation (Davies, Thomas and White, 1986; Lennmarken, Bergman, Larsson and Larsson, 1985; Vandervoort and Hayes, 1989; Vandervoort and McComas, 1986). Twitch contraction time is defined as the time from onset (of the twitch) to peak torque and half-relaxation time as the time taken from the onset to a 50 per cent reduction of peak torque (Vandervoort and Hayes, 1989). These two parameters appear to increase with advancing age and are consistent with the morphological changes that have been reported (Petrella, Cunningham, Vandervoort and Paterson, 1989).

Davies and colleagues (1986) studied the electrically evoked isometric properties of the triceps surae in young (22 years) and elderly (69 years) men and women. The results showed that the younger men and women had a decreased time to peak tension (TPT) and half-relaxation time (1/2RT) of the maximal twitch, and were 30-40 per cent stronger in terms of their MVC, when compared to the older subjects. MVF/CSA was also determined and was shown to be significantly higher in the younger subjects. This latter finding however, was ascertained through anthropometric measurements and as discussed previously will cause gross errors in estimation. Rice et al. (1989a) found that through CT scans, the plantar flexors of the elderly group contained 81 per cent more non-muscle tissue than the younger subjects. Moreover, this technique of determining cross-sectional area is unable to discern some non-muscle constituents, especially in older individuals and therefore implies that the above cited percentage may have even been higher. This would therefore probably account for the difference in MVF/CSA observed in Davies et al. (1986) investigation.

In agreement with the above results is the project conducted by Vandervoort and McComas (1986) that found increases in TPT and 1/2RT with increasing age. The gastrocnemius and soleus muscles were examined, with the lengthening of the twitch most noticeable in the former muscle. This observation was believed to be influenced via an increase in the proportion of tension developed by type I muscle fibres in the older subjects, because of the type II atrophy that occurs with age. Contraction patterns in the older individuals expressed, perhaps contrary to expectation, full recruitment of their motor unit pool, which is in line with the data produced by Phillips et al. (1992) and Vandervoort and Hayes (1989), thus excluding an important possible cause of weakness. 

RESISTANCE TRAINING – WHAT ARE THE BENEFITS?

The responses to a program of regular resistance training influence the morphological and functional characteristics of the neuromuscular system (Sale, 1988; Tesch, 1988). The adaptations made to resistance training are well documented in younger age groups (Hakkinen and Komi, 1986; Hakkinen, Alen and Komi, 1985; Hather, Tesch, Buchanan and Dudley, 1991; Kraemer, Noble, Clark, and Culver, 1987; Luthi, Howald, Claassen, Rosler, Vock and Hoppeler, 1986; Moritani and DeVries, 1979), with an increasing amount of information related to older age groups being produced (Brown, McCartney and Sale, 1990; Charette, McEvoy, Pyka, Snow-Harter, Guido, Wiswell and Marcus, 1991; Fiatarone et al., 1990; Frontera, Meredith, O’Reilly, Knuttgen and Evans, 1988; McCartney, Hicks and Martin-Gerend, 1993; Parson, Foster, Harman, Dickinson, Oliva, Westerlind and Boulder, 1992). Young men and women following resistance training programs demonstrate substantial increases in strength, hypertrophy of both type I and II muscle fibres, increases in muscle cross-sectional area and favourable neural changes (Hakkinen et al., 1985; Hather et al., 1991). With muscle strength in older persons being a significant factor that influences functional mobility (Bassey et al., 1992), it would appear that resistance training may provide an important tool in trying to combat the age-related changes in skeletal muscle, and this would consequently improve the structural and functional status of an ageing individual.

Fiatarone and associates (1990) investigated the responses to 8 weeks of high-intensity, progressive resistance training (concentric and eccentric contractions), performed 3 times per week at 80% of the one repetition maximum (1RM), in 10 frail, institutionalized elderly men and women (age= 90 +/- 1 years). Leg extensor strength prior to the program was extremely low, with a mean 1RM of 9 kilograms. No contraindications related to the resistance training program were observed, apart from one man dropping out due to a previous repaired inguinal hernia. The amount of weight that could be lifted post-training rose from 8-21 kilograms, which represented an average improvement in strength of 174 +/- 31%.

Muscle CSA was also established through computed tomography and showed an average increase of 11.7 +/- 5.0% (quadriceps: 14.5 +/- 7.8%; hamstrings and adductors: 10.6 +/- 9.1%) from baseline values. This however, did not correlate to the strength gains, thus implying that improved neural recruitment patterns were also influencing strength expression. The increment in strength made in this group of very old men and women, translated into improvements of functional mobility, with tandem gait speed rising. In addition, two subjects no longer needed canes to walk at the end of the project, with another subject being able to rise from a chair without the use of the arms (previously they were required). Although there were demonstrated improvements in muscle strength and muscle cross-sectional area, detraining resulted in a significant 32% loss of maximum strength in only 4 weeks. Clearly, some form of maintenance program would be required for the preservation of the training adaptations made following a resistance training program.

Recently, Klitgaard and co-workers (1990) produced data that suggested very strongly that resistance training performed consistently over many years may attenuate or even stop to some degree, the ‘usual’ changes evident in ageing human skeletal muscle. In this cross-sectional study 5 different groups which included young (28 +/- 0.1 years) and elderly (68 +/- 0.5 years) sedentary subjects, elderly swimmers (69 +/- 1.9 years), runners (70 +/- 0.7 years) and strength trained subjects (68 +/- 0.8 years) were investigated via the function and morphology of their knee extension/m. vastus lateralis and elbow flexion/biceps brachii. The training groups had completed their training regimens, on average, 3 times a week, for the 12-17 years prior to the study.

The results indicated that the elderly strength trained group possessed similar testing and measurement parameters to the sedentary young group. On the other hand, the swimmers, runners and inactive older groups produced results considerably different to the elderly strength trained and inactive younger groups. Maximal isometric torque (MIT), CSA and fibre typing was determined for both muscles. Maximal isometric torque in the strength trained elderly men was similar to the young sedentary subjects, in comparison to the swimmers and runners who displayed strength levels in line with age-matched controls. As a consequence, the strength trained group exhibited 72 and 38% greater knee extension and elbow flexion MIT, respectively, than the age-matched controls. The CSA measurements also demonstrated differences, with the quadriceps femoris and elbow flexors, 18 and 29% larger, respectively, in the strength trained and young sedentary groups, when compared to the swimmers, runners and sedentary older groups. The third parameter mentioned, again showed the consistency between young and strength trained groups. Mean fibre area was identical in these two groups, while all three other groups had significantly smaller mean fibre areas. The most striking finding was the extraordinary large type IIb fibres present in the strength trained group. This contrasted to the much smaller and atrophied type II fibres in all other elderly groups.

Obviously there is difficultly in establishing valid conclusions from this study due to the cross-sectional design and the relatively small number of subjects. Nevertheless, it was shown that only the strength trained elderly group maintained excellent muscle function, in comparison to the other elderly groups. This suggests that strength training performed regularly can prevent age-related decreases in strength and quantitative levels of contractile tissue.

These above observations find further support from other projects (Klitgaard et al., 1989a; Klitgaard et al., 1989b) conducted on old rat muscle, that suggested the reduced use of muscle has a major influence on the observed alterations in the morphology and function of skeletal muscle with age. Strength trained and swim trained rats enabled a comparison of two different training regimens. Both studies showed strength training had a considerable counteracting effect on the age-related, atrophy, composition and contractile properties of muscle fibres. The swim trained rats, on the other hand, displayed no evidence of any changes in these parameters, although the levels of endurance were improved. Klitgaard et al. (1989a) concluded that an altered activity pattern with increasing age, where the amount and frequency of forceful muscular contractions decreases, appears to have a profound effect on the “atrophy, weakness, and slowing of contractions, which are the normal features of ageing skeletal muscle” (1989a: 1407).

Resistive exercise and its effects on elderly women has not been addressed as frequently as in elderly men. Consequently, two recent investigations (Charette et al., 1991; Cress, Thomas, Johnson, Kasch, Cassens, Smith and Agre, 1991), assessed the capacity of older women to adapt to progressive resistance training. The study conducted by Cress et al. (1991) combined aerobic training with resistance work and proceeded for 50 weeks, while the study by Charette and associates (1991) was only 12 weeks in duration and specifically attended to resistive training. The subjects of both studies were of a similar age (approximately 70 years old) and results indicated paralleling changes in the structure and function of leg extensors (m. vastus lateralis). Strength in both training groups improved dramatically, and this was accompanied by comparable changes in type II muscle fibre areas. This increment in fibre area was especially evident in the type IIb fibres (increased 29%, maintenance of type IIa area) in Cress et al. (1991) project. These results led Charette et al. (1991) to ascribe the age-related decreases in type II fibre areas and strength alterations, to levels of physical activity, rather than, an inherent change of muscle to age.

Brown and colleagues (1990) trained the elbow flexors (biceps brachii and brachialis) in 14 elderly males for 12 weeks at an intensity of 70-90% of 1RM. This program produced a 48% increase in dynamic strength (as determined through 1RM) and 8.8% rise in isokinetic strength in the trained arm. In addition, the contralateral control arm (untrained arm) demonstrated increases of 12.7 and 6.5%, respectively, in 1RM and isokinetic strength assessment. This phenomenon has been referred to by Sale (1988) as the cross-training effect. Computed tomography after training showed that the trained arm had increased its’ cross-sectional area by 17.4%, compared to pre-training scans. In contrast, there was a small, but nevertheless, significant increase in the cross-sectional area of the untrained arm.

These results that demonstrate increments in strength in the untrained arm, with no appreciable increase in cross-sectional area, suggest that neural adaptations need to be included in the explanation for the observed changes. Muscle fibre areas also altered in the trained and untrained arm. Type II fibres of the trained arm increased approximately 3-fold compared to the untrained arm (30.2% versus 10.7%), with type I fibres increasing, but to a smaller degree in both the trained and untrained arms (percentages not reported). This finding of greater hypertrophy in type II fibres is consistent with other studies (Hather et al., 1991), however, there is still some discordance in relation to whether type I fibre enlargement occurs, following resistance exercise in elderly males and females, due to the conflicting results of several projects (Larsson, 1982; Frontera et al., 1988; Charette et al., 1991).

Progressive resistance training in older individuals has been been shown to increase strength and produce significant hypertrophy, provided the program is of sufficient intensity, duration and frequency (Brown et al., 1990; Charette et al., 1991). These alterations have been associated with enhanced functional mobility, thus maintaining older person’s independence (Fiatarone et al., 1990). With adaptations and recovery rates (Clarkson and Dedrick, 1988) to resistance training in elderly and younger groups being similar in nature, the alterations in muscle morphology and function can no longer be viewed as an inevitable consequence of ageing (Rogers and Evans, 1993). Intervention resistive programs or adherence to some form of resistance exercise over time, may result in an attenuation of the age-related changes in skeletal muscle, and hence decrease the atrophy, weakness and slowing of contractions, with ‘normal’ inactive ageing (Klitgaard et al., 1990; Klitgaard et al., 1989a).

CONCLUSIONS

Changes in muscle morphology and function occur as a result of ageing. However, whether ageing per se can fully account for the significant decrements in muscle volume and muscle strength is disputable. It would appear that declining activity levels and a reduction in muscular contractions forceful in nature play a far greater role than previously thought. Evidence suggests that these age-related changes are not just biologically driven either because data shows that Western societies harbour sociocultural expectations that physical activity levels should decrease proportionally to age. In other words, high-intensity physical activity and resistance training are perceived as inappropriate for older adults, with the inappropriateness increasing commensurate to advancing age.

The accelerating reduction of muscle volume after the sixth decade of life, may be mediated through selective atrophy of type II muscle fibres and a highly significant decrease in fibre number. Fibre compositional alterations in favour of type I expression remain contentious, with inconsistent data exacerbating the difficulty of establishing a consensus. The large decline in fibre number is probably the main determinant of the large reduction in muscle cross-sectional area. These changes are mainly attributable to the accelerating loss of functioning motor units via a continuous neurogenic denervation/reinnervation process.

Strength decrements with age have been predominantly ascribed to muscle cross-sectional area changes. Many confounding variables, however, make the assessment of the underlying reasons for the changes in muscle function very difficult to determine. Until further data is produced, strength decreases will be seen as mainly due to the reduction in muscle mass and therefore, muscle cross-sectional area.

Resistance training is now acknowledged as an excellent form of exercise to attenuate the age-related alterations in human skeletal muscle morphology and function. Hypertrophy and strength gains have been demonstrated to be similar in young and older subjects. Likewise, the recovery abilities for young versus old following resistive exercise have been shown to similar. In light of these most promising benefits, it is suggested that the maintenance of activity levels, including some form of resistance training exercise, should be performed with increasing age.  

REFERENCES

ANIANSSON, A., HEDBERG, M., HENNING, G.B. and GRIMBY, G. (1986). “Muscle morphology, enzymatic activity, and muscle strength in elderly men: A followup study.” Muscle and Nerve. 9: 585-591.

ANIANSSON, A., ZETTERBERG, C., HEDBERG, M. and HENRIKSSON, K.G. (1984). “Impaired muscle function with ageing- A background factor in the incidence of fractures of the proximal end of the femur.” Clinical Orthopaedics and Related Research. 191: 193-201.

AOYAGI, Y. and SHEPHARD, R.J. (1992). “Ageing and Muscle Function.” Sports Medicine. 14(6): 376-396.

BASSEY, E.J. and SHORT, A.H. (1990). “A new method for measuring power output in a single leg extension: feasibility, reliability and validity.” European Journal of Applied Physiology and Occupational Physiology. 60: 385-390.

BASSEY, E.J., FIATARONE, M.A., O’NEILL, E.F., KELLY, M., EVANS, W.J. and  LIPSITZ, L.A. (1992). “Leg extensor power and functional performance in very old men and women.” Clinical Science. 82: 321-327.

BELANGER, A.Y. and McCOMAS, A.J. (1981). “Extent of motor unit activation during effort.” Journal of Applied Physiology. 51(5): 1131-1135.

BORTZ, W.M. (1982). “Disuse and ageing.” Journal of American Medical Association. 248(10): 1203-1208.

BROWN, W.F., STRONG, M.J. and SNOW, R. (1988). “Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with ageing.” Muscle and Nerve. 11: 423-432.

BROWN, A.B., McCARTNEY, N. and SALE, D.G. (1990). “Positive adaptations to weight-lifting training in the elderly.” Journal of Applied Physiology. 69(5): 1725-1733.

BUSKIRK, E.R. and SEGAL, S.S. (1989). “The ageing motor system: Skeletal muscle weakness.” in Waneen W. SPIRDUSO and Helen M. ECKERT (Eds.) Physical Activity and Ageing. Champaign, Illinois: Human Kinetics Publishers: 19-36.

CHARETTE, S.L., McEVOY, L., PYKA, G., SNOW-HARTER, C., GUIDO, D., WISWELL, R.A. and MARCUS, R. (1991). “Muscle hypertrophy response to resistance training in older women.” Journal of Applied Physiology. 70(5): 1912-1916.

CLARKSON, P.M., KROLL, W. and MELCHIONDA, A.M. (1981). “Age, isometric strength, rate of tension development and fiber type composition.” Journal of Gerontology. 36(6): 648-653.

CLARKSON, P.M. and DEDRICK, M.E. (1988). “Exercise-induced muscle damage, repair, and adaptation in old and young subjects.” Journal of Gerontology. 43(4): M91-M96.

COGGAN, A.R., SPINA, R.J., KING, D.S., ROGERS, M.A., BROWN, M., NEMETH, P.M and HOLLOSZY, J.O. (1992). “Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women.” Journal of Gerontology. 46B: 71-76.

CRESS, M.E., THOMAS, D.P., JOHNSON, J., KASCH, F.W., CASSENS, R.G., SMITH, E.L. and AGRE, J.C. (1991). “Effect of training on VO2 max, thigh strength, and muscle morphology in septuagenarian.” Medicine and Science in Sports and Exercise. 23(6): 752-758.

CUNNINGHAM, D.A., MORRISON, D., RICE, C.L. and COOKE, C. (1987). “Ageing and isokinetic plantar flexion.” European Journal of Applied Physiology and Occupational Physiology. 56: 24-29.

DANNESKIOLD-SAMSOE, B., KOFOD, V., MUNTER, J., GRIMBY, G., SCHNOHR, P. and JENSEN, G. (1984). “Muscle strength and functional capacity in 78-81-year-old men and women.” European Journal of Apllied Physiology and Occupational Physiology. 52: 310-314.

DAVIES, C.T.M., THOMAS, D.O. and WHITE, M.J. (1986). “Mechanical properties of young and elderly human muscle.” Acta Medica Scandinavica Suppl. 711: 219-226.

EVANS, W.J. (1992). “Exercise, nutrition and ageing.” Journal of Nutrition. 122: 796-801.

FIATARONE, M.A., MARKS, E.C., RYAN, N.D., MEREDITH, C.N., LIPSTIZ, L.A.and EVANS, W.J. (1990). “High-Intensity Strength Training in Nonagenarians- Effects on Skeletal Muscle.” Journal of the American Medical Association. 263: 3029-3034.

FRONTERA, W.R., HUGHES, V.A., LUTZ, K.J. and EVANS, W.J. (1991). “A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women.” Journal of Applied Physiology. 71(2): 644-650.

FRONTERA, W.R., MEREDITH, C.N., O’REILLY, K.P., KNUTTGEN, H.G. and EVANS, W.J. (1988). “Strength conditioning in older men: skeletal muscle hypertrophy and improved function.” Journal of Applied Physiology. 64(3): 1038-1044.

GREIG, C.A, BOTELLA, J. and YOUNG, A. (1993). “The quadriceps strength of healthy elderly people remeasured after eight years.” Muscle and Nerve. 16: 6-10.

GRIMBY, G., DANNESKIOLD-SAMSOE, B., HVID, K. and SALTIN, B. (1982). “Morphology and enzymatic capacity in arm and leg muscles in 78-81 year old men and women.” Acta Physiologica Scandinavica. 115: 125-134.

HAKKINEN, K., ALEN, M. and KOMI, P.V. (1985). “Changes in isometric force- and relaxation-time, eletromyographic and muscle fiber characteristics of human skeletal muscle during strength training and detraining.” Acta Physiologica Scandinavica. 125: 573-585.

HAKKINEN, K. and KOMI, P.V. (1986). “Training-induced changes in neuromuscular performance under voluntary and reflex conditions.” European Journal of Applied Physiology. 55: 147-155.

HAKKINEN, K. and KOMI, P.V. (1983). “Electromyographic changes during strength training and detraining.” Medicine and Science in Sports and Exercise. 15(6): 455-460.

HATHER, B.M., TESCH, P.A., BUCHANAN, P. and DUDLEY, G.A. (1991). “Influence of eccentric actions on skeletal muscle adaptations to resistance training.” Acta Physiologica Scandinavica. 143: 177-185.

HEYMSFIELD, S.B., ARTEAGA, C., McMANUS, C., SMITH, J. and MOFFIT, S. (1983). “Measurement of muscle mass in humans: validity of the 24-hour urinary creatinine method.” American Journal of Clinical Nutrition. 37: 478-494.

HICKS, A.L., CUPIDO, C.M., MARTIN, J. and DENT, J. (1991). “Twitch potentiation during fatiguing exercise in the elderly: the effects of training.” European Journal of Applied Physiology and Occupational Physiology. 63: 278-281.

KALLMAN, D.A., PLATO, C.C. and TOBIN, J.D. (1990). “The role of muscle loss in the age-related decline of grip strength: Cross-sectional and longitudinal perspectives.” Journal of Gerontology. 45(3): M82-88.

KAUFFMAN, T.L. (1985). “Strength training effects in young and aged women.” Archives of Physical Medicine and Rehabilitation. 66: 223-226.

KLITGAARD, H., MANTONI, M., SCHIAFFINO, S., AUSONI, S., GORZA, L., LAURENT-WINTER, C., SCHNOHR, P. and SALTIN, B. (1990). “Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds.” Acta Physiologica Scandinavica. 140: 41-54.

KLITGAARD, H., MARC, R., BRUNET, A., VANDEWALLE, H. and MONOD, H. (1989a). “Contractile properties of old rat muscles: effect of increased use.” Journal of Applied Physiology. 67(4): 1401-1408.

KLITGAARD, H., BRUNET, A., MATON, B., LAMAZIERE, C., LESTY, C. and MONOD, H. (1989b). “Morphological and biochemical changes in old rat muscles: effect of increased use.” Journal of Applied Physiology. 67(4): 1409-1417.

KOMI, P.V. (1988). “The musculoskeletal system” in Albert DIRIX, Howard G. KNUTTGEN and Kurt TITTEL (Eds) The Olympic Book of Sports Medicine- Volume 1. Victoria, Australia: Blackwell Scientific Publications.

KRAEMER, W.J., NOBLE, B.J., CLARK, M.J. and CULVER, B.W. (1987). “Physiologic responses to heavy-resistance exercise with very short rest periods.” International Journal of Sports Medicine. 8: 247-252.

LARSSON, L. (1982). “Physical training effects on muscle morphology in sedentary males at different ages.” Medicine and Science in Sports and Exercise. 14(3): 203-206.

LARSSON, L., GRIMBY, G. and KARLSSON, J. (1979). “Muscle strength and speed of movement in relation to age and muscle morphology.” Journal of Applied Physiology. 46(3): 451-456.

LARSSON, L., SJODIN, B. and KARLSSON, J. (1978). “Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22-65 years.” Acta Physiologica Scandinavica. 103: 31-39.

LARSSON, L. and KARLSSON, J. (1978). “Isometric and dynamic endurance as a function of age and skeletal muscle charateristics.” Acta Physiologica Scandinavica. 104: 129-136.

LENNMARKEN, C., BERGMAN, T., LARSSON, J. and LARSSON, L.-E. (1985). “Skeletal muscle function in man: force, relaxation rate, endurance and contraction time-dependance on sex and age.” Clinical Physiology. 5: 243-255.

LEXELL, J. and TAYLOR, C.C. (1991). “Variability in muscle fibre areas in whole human quadriceps muscle: effects of increasing age.” Journal of Anatomy. 174: 239-249.

LEXELL, J., DOWNHAM, D. and SJOSTROM, M. (1986). “Distribution of different  fibre types in human skeletal muscles- Fibre type arrangement in m. vastus lateralis from three groups of healthy men between 15 and 83 years.” Journal of the Neurological Sciences. 72: 211-222.

LEXELL, J., TAYLOR, C.C. and SJOSTROM, M. (1988). “What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in the whole vastus lateralis muscle from 15- to 83-year-old men.” Journal of the Neurological Sciences. 84: 275-294.

LEXELL, J. (1993). “Ageing and human muscle: Observations from Sweden.” Canadian Journal of Applied Physiology. 18(1): 2-18.

LEXELL, J. and DOWNHAM, D. (1992). “What is the effect of ageing on type 2 muscle fibers ? ” Journal of the Neurological Sciences. 107: 250-251.

LUTHI, J.M., HOWARD, H., CLAASSEN, H., ROSLER, K., VOCK, P. and HOPPELER, H. (1986). “Structural Changes in Skeletal Muscle Tissue with Heavy-Resistance Exercise.” International Journal of Sports Medicine. 7(3): 123-127.

McARDLE, W.D., KATCH, F.I. and KATCH, V.L. (1986). Exercise Physiology- Energy, Nutrition, and Human Performance. Philadelphia, United States of America: Lea and Febiger.

McCARTNEY, N., HICKS, A. and MARTIN-GEREND, J. (1993). “The time course of strength changes over 10 months of weight lifting training in elderly adults.” Medicine and Science in Sports and Exercise. 25(5): S130 (Abstract).

MEREDITH, C.N., FRONTERA, W.R., O’REILLY, K.P. and EVANS, W.J. (1992). “Body composition in elderly men: Effect of dietary modification during strength training.” Journal of American Geriatrics Society. 40(2): 155-162.

MUNNINGS, F. (1993). “Strength training- Not only for the young.” The Physician and Sportsmedicine. 21(4): 132-140.

OERTEL, G. (1986). “Changes in human skeletal muscles due to ageing- Histological and histochemical observations on autopsy material.” Acta Neuropathologica. 69: 309-313.

OSTROW, A.C., JONES, D.C. and SPIKER, D.D. (1981). “Age role expectations and sex role expectations for selected sport activities.” Research Quarterly for Exercise and Sport. 52(2): 216-227.

OSTROW, A.C. and DZEWALTOWSKI, D.A. (1986). “Older adults’ perceptions of physical activity participation based on age-role and sex-role appropriateness.” Research Quarterly for Exercise and Sport. 57(2): 167-169.

OSTROW, A.C., KEENER, R.E. and PERRY, S.A. (1987). “The age grading of physical activity among children.” International Journal of Ageing and Human Development. 24(2): 101-111.

OVEREND, T.J., CUNNINGHAM, D.A., KRAMER, J.F., LEFCOE, M.S. and PATERSON, D.H. (1992). “Knee extensor and knee flexor strength: Cross-sectional area ratios in young and elderly men.” Journal of Gerontology. 47(6): M204-M210.

PARSONS, D., FOSTER, V., HARMAN, A., DICKINSON, A., OLIVA, P. and WESTERLIND, K. (1992). “Balance and strength changes in elderly subjects after heavy-resistance strength training.” Medicine and Science in Sports and Exercise. 24(5): S21 (Abstract).

PETRELLA, R.J., CUNNINGHAM, D.A., VANDERVOORT, A.A. and PATERSON, D.H. (1989). “Comparison of twitch potentiation in the gastrocnemius of young and elderly men.” European Journal of Applied Physiology and Occupational Physiology. 58: 395-399.

PHILLIPS, S.K., BRUCE, S.A., NEWTON, D. and WOLEDGE, C. (1992). “The weakness of old age is not due to failure of muscle activation.” Journal of Gerontology. 47(2): M45-49.

RICE, C.L., CUNNINGHAM, D.A., PATERSON, D.H. and LEFCOE, M.S. (1989a). “Arm and leg composition determined by computed tomography in young and elderly men.” Clinical Physiology. 9: 207-220.

RICE, C.L., CUNNINGHAM, D.A., PATERSON, D.H. and RECHNITZER, P.A. (1989b). “Strength in an Elderly Population.” Archives of Physical Medicine and Rehabilitation. 70: 391-397.

ROGERS, M.A. and EVANS, W.J. (1993). “Changes in skeletal muscle with ageing: Effects of exercise training.” in John O. HOLLOSZY (Ed.) Exercise and Sports Sciences Reviews. Baltimore, United States of America: Williams & Wilkins: Vol. 6: 65-102.

SALE, D.G. (1988). “Neural adaptation to resistance training.” Medicine and Science in Sportsd and Exercise. 20(5): S135-S145.

SCELSI, R., MARCHETTI, C. and POGGI, P. (1980). “Histochemical and ultrastructural aspects of M. vastus lateralis in sedentary old people (age 65-89 years).” Acta Neuropathologica. 51: 99-105.

SHELLEY, A., SNOW-HARTER, C., ROBINSON, T., WEGNER, M. and SHAW, J. (1993). “The relationship between isokinetic strength and age in a large cross section of healthy women.” Medicine and Science in Sports and Exercise. 25(5): S161.

SIPILA, S. and SUOMINEN, H. (1991). “Ultrasound imageing of the quadriceps muscle in elderly athletes and untrained men.” Muscle and Nerve. 14: 527-533.

SIPILA, S. and SUOMINEN, H. (1993). “Muscle ultrasonography and computed tomography in elderly trained and untrained women.” Muscle and Nerve. 16: 294-300.

STALBERG, E., BORGES, O., ERICSSON, M., ESSEN-GUSTAVSSON, B., FAWCETT, P.R.W., NORDESJO, L.O., NORDGREN, B. and UHLIN, R. (1989). “The quadriceps femoris muscle in 20-70-year-old subjects: Relationship between knee extension torque, electophysiological parameters, and muscle fibre characteristics.” Muscle and Nerve. 12: 382-389.

TESCH, P.A. (1988). “Skeletal muscle adaptation consequent to long-term heavy resistance exercise.” Medicine and Science in Sports and Exercise. 20(5): S132-S134.

TRAPPE, S.W., COSTILL, D.L., FINK, W.J., PEARSON, M.D. and VUKOVICH, M.D. (1993). “Effects of ageing on muscle morphology: A longitudinal analysis.” Medicine and Science in Sports and Exercise. 25(5): S161 (Abstract).

VANDERVOORT, A.A. (1992). “Effects of ageing on human neuromuscular function: Implications for exercise.” Canadian Journal of Applied Sport Sciences. 17(3): 178-184.

VANDERVOORT, A.A., KRAMER, J.F. and WHARRAM, E.R. (1990). “Eccentric knee strength of elderly females.” Journal of Gerontology. 45(4): B125-B128.

VANDERVOORT, A.A. and HAYES, K.C. (1989). “Plantarflexor muscle function in young and elderly women.” European Journal of Applied Physiology and Occupational Physiology. 58: 389-394.

VANDERVOORT, A.A. and McCOMAS, A.J. (1986). “Contractile changes in opposing muscles of the human ankle joint with ageing.” Journal of Applied Physiology. 61(1): 361-367.

WOKKE, J.H.J., JENNEKENS, F.G.I., van den OORD, C.J.M., VELDMAN, H., SMIT, L.M.E. and LEPPINK, G.J. (1990). “Morphological changes in the human end plate with age.” Journal of the Neurological Sciences. 95: 291-310.

YOUNG, A., STOKES, M. and CROWE, M. (1984). “Size and strength of the quadriceps muscles of old and young women.” European Journal of Clinical Investigation. 14: 282-287.

This literature review was conducted in 1994 as part of a proposed PhD study.

---

For local Townsville residents interested in FitGreyStrong’s Exercise Physiology services or exercise programs designed to improve muscular strength, physical function (how you move around during the day) and quality of life or programs to enhance athletic performance, contact FitGreyStrong@outlook.com or phone 0499 846 955 for a confidential discussion.

For other Australian residents or oversees readers interested in our services, please see here.

---

Disclaimer: All contents of the FitGreyStrong website/blog are provided for information and education purposes only. Those interested in making changes to their exercise, lifestyle, dietary, supplement or medication regimens should consult a relevantly qualified and competent health care professional. Those who decide to apply or implement any of the information, advice, and/or recommendations on this website do so knowingly and at their own risk. The owner and any contributors to this site accept no responsibility or liability whatsoever for any harm caused, real or imagined, from the use or distribution of information found at FitGreyStrong. Please leave this site immediately if you, the reader, find any of these conditions not acceptable.

© FitGreyStrong