Discussion
The current study permits some important insights into countermeasure exercise prescription. The flywheel exercise countermeasure was effective, compared with control, in preventing or reducing atrophy in the monoarticular knee extensors (vasti), mono articular hip extensors (adductor magnus) and ankle dorsiflexors/toe flexors. The actual exercise time was 7–9 min ‘time under tension’ with 20 min total training time including rest breaks. Importantly, these findings underscore19 that a short duration, high load, resistance exercise programme can be very effective in reducing muscle atrophy in bed-rest. Previous studies that have implemented low load, non-specific muscle exercises, were unsuccessful at reducing muscle atrophy: whole body vibration in standing in a squat position without exercise did not impact lower limb muscle atrophy,17 nor did whole body vibration implemented in supine position prevent spinal muscle atrophy.24 Furthermore, exercise protocols involving aerobic-based cycling25 and lower body negative pressure26 were largely ineffective at reducing lower limb muscle atrophy. An ergometer-based cycling exercise27 can be effective in reducing lower limb suspension induced muscle atrophy when higher intensities, and hence need for higher force muscle contraction, are implemented.
The countermeasure programme did not have an impact on atrophy in the hamstrings, which are important for ambulation. Of the hamstrings, semimembranosus and biceps femoris long head are primarily hip extensors28 with semitendinosus playing more of a role in control of knee flexion.29 30 In contrast, another research group11 reported complete prevention of hamstring muscle atrophy due to their resistance exercise protocol in 20 days bed-rest when the leg press exercise was performed up to 110° of hip flexion. This underscores the need for greater specificity of exercise prescription for the hamstrings.
Maintenance of the calf musculature in disuse bed-rest via exercise has, in a number of studies, proven difficult. In the current study the atrophy of the calf muscles was significantly reduced, but muscle atrophy still occurred: 20% of soleus muscle volume was lost in the flywheel group compared with 29% loss in the inactive group at the end of bed-rest. Prior work does suggest that higher volumes of calf muscle exercise do appear to have a greater protective effect: when resistive vibration exercise including calf press exercises was performed three times a week,19 15% loss in soleus muscle volume after 56 days of bed-rest was observed, compared with 7% loss in soleus muscle volume after 56 days of bed-rest in another study2 where resistive vibration exercise was performed 11 times a week. However, for the calf muscles, there is evidence in the literature31 that attaining hypertrophy in ambulant exercise studies is more difficult with standard hypertrophy protocols than it is for the knee extensors. This is in line with the notion that muscles that are typically load-bearing in daily life are more difficult to hypertrophy than non-load-bearing muscles.32 Investigation of other exercise modes, such as treadmill running or jumping exercises, is needed to improve exercise prescription for preventing disuse atrophy of the calf musculature.
Recovery of muscle volume occurred in all muscles by 90 days after prolonged bed-rest. We observed, however, increase of muscle volume over and beyond the prebed-rest baseline volume in the inactive subjects in the long term after bed-rest. Importantly, this effect was observed in major muscle groups and not just in minor and/or small muscle groups. The time subjects spent lying supine prior to MR-scanning was strictly controlled in this study. Also, this effect was seen only in the inactive subjects, not in the flywheel exercise subjects (figure 2). We can therefore rule out a systematic, confounding, effect particular to the current study. In further support of our interpretation, peripheral quantitative CT examinations were performed in the same collective33 and these investigations also showed significant increases in lower leg muscle area 90 days and beyond after bed-rest. After another 56 days bed-rest study performed at a different facility,34 the authors observed a statistical trend towards an overshoot of calf musculature area recovery after bed-rest, again specific to the inactive group, but not the exercise group, of that study. While we cannot be certain that this muscle hypertrophy involved true muscle fibre hypertrophy, we did not see any association between these muscle volume increases in the long term after bed-rest with improvements in countermovement jump performance.
Finally, of the muscles active in the hip joint, the quadratus femoris showed the fastest rate and extent, of atrophy. When we observed this in a prior bed-rest study,35 we were not sure if this was a chance finding. In a recent cadaver study, one group concluded that quadratus femoris is a primary extensor of the hip when it is in a flexed position.36 In line with this, recent fine-wire electromyography findings37 found that quadratus femoris shows a peak of activity in walking and running during the first part of stance (ie, when the flexed hip begins to bear load) and also in late swing phase in running, presumably to decelerate the flexing hip during late swing. Overall, the recent finding shows that quadratus femoris is important for load-bearing and control of extension force at the hip joint, particularly in a flexed position. This helps to understand why quadratus femoris in particular is affected in disuse.
It is important to mention limitations of the current work. As is typical of bed-rest studies in Europe, only one gender was included in the study in an effort to reduce intersubject variability. As such, we cannot be certain that our results are applicable to female bed-rest participants. The number of subjects was limited due to logistical and financial restraints. Due to the limited number of subjects, some non-significant results for the effect of the exercise protocol may represent false negatives. For some smaller muscles, such as adductor brevis and obturator externus, reproducibility of the measurements is not as high as for larger muscle groups and non-significant findings for these muscles might be false negatives. Even though the current study provides important evidence for exercise prescription in astronauts, application of the current protocols to spaceflight could not occur on a 1:1 basis.
In conclusion, the current study investigated the impact of 90 days bed-rest on atrophy of the muscles of the lower limb, the impact of a flywheel exercise countermeasure, and the recovery of the musculature after bed-rest. The greatest rates and extent of atrophy was seen in the soleus and gastrocnemius medialis, followed by the gastrocnemius lateralis, peroneals, vasti, biceps femoris long head, other posterior calf musculature, semimembranosus, anterior tibial muscles, adductor magnus and quadratus femoris. The flywheel exercise countermeasure was effective, compared with control, in preventing or reducing atrophy in the vasti, adductor magnus and ankle dorsiflexors/toe flexors. Thus, a short-duration high-intensity resistance exercise programme performed every third day can be effective in preventing muscle atrophy in disuse. The countermeasure was, however, not effective in preventing atrophy of the hamstrings, medial thigh muscles, ankle evertors and dorsiflexors. Finally, in the long term after bed-rest we saw that inactive subjects exhibited an overshoot of muscle volume recovery in some muscle groups compared with before bed-rest.