The main finding of the present study is that superimposing endurance training on a regular resistance exercise programme of highly resistance-trained younger and older men induces an increase in muscle oxidative capacity without a decrement in muscle (fibre) size in both age groups that was accompanied by angiogenesis. This suggests that even in older people highly trained for strength, benefits of endurance exercise do not impair force production or lead to reductions in muscle size.
We observed that even when maintaining high levels of resistance exercise, there is still an age-related reduction in muscle mass, absolute maximal oxygen consumption (L·min
−1) and muscle strength. This is also reported in elite master weightlifters where the relative rate of age-related decline in muscle power was similar to that of control subjects, but they still had a larger muscle power compared to age-matched control subjects (Pearson et al.
2002). This phenomenon is not limited to power athletes but the exercise performance in all athletic disciplines shows an age-related decline (Ganse et al.
2018) that in endurance athletes was associated with an age-related reduction in VO
2max at a similar relative rate to untrained subjects (Tanaka and Seals
2008).
Here, we showed that also in highly resistance-trained men the absolute VO
2max decreased with age, but the VO
2max per kg body mass was similar in younger and older participants, suggesting that the decline in VO
2max with ageing is largely due to a loss of muscle mass (Fleg and Lakatta
1988). This is further supported by our observation of a positive relationship between quadriceps ACSA and VO
2max.
The lower MVC torque in older compared to younger participants seems to be largely due to a loss of muscle mass. The higher OD of muscle in the MRI images of older participants suggests that they have greater levels of intramuscular fat when compared to younger subjects. The accumulation of intramuscular fat during ageing can reach levels of more than 10% (Schwenzer et al.
2009) and may result in a reduced specific tension that will further contribute to the lower muscle strength (McPhee et al.
2018). Yet, we observed that the specific torque (MVC torque per ACSA) was similar in our younger and older participants. The similar specific force (per ACSA) may be explained by the reduction in pennation angle that accompanies the decrease in muscle size during ageing, where the fascicles are more in line of pull of the tendon (Degens et al.
2009). Alternatively, the maintenance of specific tension in our resistance-trained participants suggests that although resistance training cannot prevent the age-related reductions in muscle size, it may help to maintain the ‘muscle quality’ or force per unit area of muscle (Reeves et al.
2004).
The smaller muscle ACSA was probably more related to a reduction in fibre number that has often been reported during ageing (McPhee et al.
2018) than a decrease in fibre size, as we did not find a significant difference in FCSA between younger and older highly resistance-trained men. Such an absence of an age-related reduction in FCSA was also seen in master endurance cyclists (Pollock et al.
2018), but not in master sprinters (Korhonen et al.
2006). Whatever the cause of the discrepancy, these observations suggest that regular exercise may attenuate the age-related fibre atrophy, but not the age-related loss of muscle fibres, corresponding with the observation that motor unit loss is not attenuated in longstanding master athletes (Piasecki et al.
2019).
We found that the biopsies of our 61- to 77-year-old participants exhibited a greater proportion of type I fibres than the younger group, similar to the increased proportion of type I fibres found in muscles from older people (Larsson et al.
1978). This is, however, an equivocal finding, as others have reported no significant age-related change in the fibre type composition of the
m. vastus lateralis (Andersen
2003; Barnouin et al.
2017).
Similar to what has been found in the recreationally active population (Barnouin et al.
2017), the capillarisation of the muscles from our older highly resistance-trained men was lower than that found in younger participants. Since blood flow is, via shear stress, an important factor for the maintenance of the vascular bed (Hudlicka et al.
1992), the age-related capillary rarefaction may be due to a reduction in sheer stress resulting from impaired vasodilation and blood flow responses in ageing (Proctor and Parker
2006).
Is there a concurrent training effect?
Endurance exercise has long been associated with atrophy of type I and type II fibres and an increase in muscle oxidative capacity (Kraemer
1995; Baar
2006; Staron et al.
1984), and therefore has been thought to diminish the resistance training-induced hypertrophy via the so-called concurrent training effect (Hickson
1980). It is possible however, that this is due to non-functional overreaching through excessive training frequencies, intensities and volumes, as others have found comparable outcomes in combined training groups to those subjected to resistance training only when moderate frequencies and intensities were used (McCarthy et al.
1995).
The inverse relationship between fibre size and oxidative capacity suggests that there is a trade-off between fibre size and oxidative capacity (van Wessel et al.
2010; van der Laarse et al.
1998), where due to this trade-off, the endurance exercise-induced increase in oxidative capacity may cause muscle fibre atrophy. Yet, we have seen in rodent studies that this constraint on fibre size may be broken. For instance, hyper-muscular myostatin null mice overexpressing oestrogen-related receptor gamma (Errγ) have a similar fibre size as the myostatin null mice, yet with an elevated oxidative capacity (Omairi et al.
2016), and hypertrophy of overloaded mouse plantaris muscles was accompanied by an increase in oxidative capacity (Ballak et al.
2016). However, the hypertrophied fibres in the muscles of these mice are still smaller (1500 µm
2 in Ballak et al. (
2016)) or the same size (up to 4000 µm
2 in type IIb fibres; (Omairi et al.
2016)) than untrained human muscle fibres (4000 µm
2; (Barnouin et al.
2017; Wust et al.
2009)). It could thus be that the size constraint is not yet reached, and that only in highly resistance-trained men with much larger fibres (8000 µm
2 in our younger group) any increase in oxidative capacity will constrain fibre size and induce atrophy. While we found that endurance training added to the regular resistance exercise of highly resistance-trained men induced an increase in oxidative capacity, this was not accompanied by a reduction in FCSA. These observations challenge the concept of a trade-off between fibre size and oxidative capacity.
There are several potential explanations for this apparent violation of the size constraint, such as a flattening of the fibres to reduce diffusion distances from the periphery to the core of the fibre, increased myoglobin levels to maintain oxygen availability to mitochondria even at low oxygen tension, movement of mitochondria to the periphery of the fibre and/or angiogenesis (Hendrickse and Degens
2019). As in oxidative, more than in glycolytic, fibres mitochondria are more concentrated in the sub-sarcolemmal region (Wust et al.
2009), such a redistribution could also occur when endurance training is superimposed on resistance exercise. However, redistributing mitochondria to the sub-sarcolemmal region creates longer diffusion distances for ATP from the mitochondria to the ATP-consuming myofibrils in the core of the fibre (Kinsey et al.
2007) that could put in turn put a diffusion limit on fibre size (Degens
2012). It remains to be seen, however, whether such a redistribution occurred in our population. We did not see, however, any change in the form factor of the fibres, indicating no significant change in the shape of the fibres, e.g. to a flattened shape to decrease diffusion distances, but we did see a significant increase in the number of capillaries around a fibre, in particular around type I fibres. A similar situation was seen in hypertrophied mouse plantaris where the increase in oxidative capacity and fibre size was accompanied by angiogenesis, and the attenuated hypertrophy in older mice was associated with impaired angiogenesis (Ballak et al.
2016; Hendrickse et al.
2020). In the current study, we did not find evidence for an attenuated angiogenic response in the older highly resistance-trained men, similar to that seen in older women (Gavin et al.
2015). Thus, angiogenesis in our population may well have served to ensure an adequate oxygenation in the face of an increased oxidative capacity and helped to overcome the size constraint in both younger and older highly resistance-trained men.
Muscle capillarisation may well be a determining factor in hypertrophy, as indicated by the attenuated hypertrophy in overloaded muscles from older mice that was associated with impaired angiogenesis (Ballak et al.
2016; Hendrickse et al.
2020) and the lower hypertrophic response to resistance training in muscles with lower capillary density, particularly in older adults (Snijders et al.
2017; Moro et al.
2019). Based on these and the observations in the present study, we propose that endurance training prior to a dedicated resistance-training-only programme may augment increases in muscle mass by preventing diffusion limitations (Hendrickse and Degens
2019).
At first glance, the increase in muscle oxidative capacity without a concomitant rise in VO
2max post training is difficult to understand, but VO
2max is limited by the cardiovascular system and not by the working muscle (McPhee et al.
2009). In addition, our data are in line with another study where the change in VO
2max did not correlate with the change in muscle SDH concentration after an endurance-training programme (McPhee et al.
2011). Here, we thus have muscular adaptations to the superimposed endurance-training programme, but apparently no, or only minimal cardiac adaptations. We have no explanation for this observation, but it could be that the weekly duration of the endurance training programme did not reach the threshold required for cardiovascular and cardiac adaptations to occur (Fagard
2003). Another possibility to induce such adaptations is the use of high-intensity endurance training, but then the risk of CTE may indeed develop (Sousa et al.
2019). Our study shows that endurance training of moderate duration elicits beneficial effects without inducing loss of muscle mass in resistance-trained people.