Passive Strategies for the Prevention of Muscle Wasting During Recovery from Sports Injuries
Recovery from sport injuries commonly involves a muscle disuse situation (i.e., reduction in physical activity levels sometimes preceded by joint immobilization) with subsequent negative effects on muscle mass and function.
To summarize the current body of knowledge on the effectiveness of different physical strategies that are currently available to mitigate the negative effects of muscle disuse during recovery from sports injury.
A narrative review was conducted to summarize the information available on neuromuscular electrical stimulation (NMES), blood flow restriction (BFR) and vibration intervention.
The concomitant application of BFR and low-intensity exercise has shown promising results in the prevention of disuse-induced muscle atrophy. Some benefits might also be obtained with BFR alone (i.e., with no exercise), but evidence is still inconclusive. NMES, which can be applied both passively and synchronously with exercise, can also attenuate most of the negative changes associated with disuse periods. In turn, the mechanical stimulus elicited by vibration seems effective to reduce the loss of bone mineral density that accompanies muscle disuse and could also provide some benefits at the muscle tissue level.
Different physical strategies are available to attenuate disuse-induced negative consequences during recovery from injury. These interventions can be applied passively, which makes them feasible during the first stages of the recovery. However, it would be advisable to apply these strategies in conjunction with low-intensity voluntary exercise as soon as this is feasible.
KeywordsSkeletal muscle Rehabilitation Training Muscle wasting Immobilization Injury
The risk of musculoskeletal injuries is inherent in exercise practice and especially competitive sport. Injuries and the subsequent recovery period can lead to several negative consequences not only for the athlete—including physical, psychological and societal complications—but also for the team, especially at a tactical level as the injured athlete must temporarily refrain from competition [14, 32].
The physical consequences of a sports injury vary depending upon its nature and severity. However, most injuries result in a temporary cessation (or at least a reduction) of activity although sometimes an immobilization period might also be needed during the first phase of recovery. More than half of sports injuries result in at least 1 week of exercise restriction, with 20% of competition injuries being associated with 3 or more weeks of inactivity or premature termination of the competition season . Knee injuries (particularly, anterior cruciate ligament [ACL] injury) are the most prevalent type of injury in many sports  and are usually associated with longer duration of recovery , which in turn can include an initial phase with joint immobilization .
Prolonged physical inactivity or immobilization periods during recovery from injury can result in several negative consequences for the athlete’s health. The skeletal muscle is a highly plastic tissue that is capable of altering its phenotype in response to environmental stimuli . Whereas an increase in mechanical loading stimulates the hypertrophic processes, unloading situations or periods of inactivity such as those needed to recover from sports injuries result in muscle atrophy . Disuse periods as short as 5 days, which are common after sport injuries, have proven to elicit significant negative consequences in young subjects, including a substantial loss of muscle mass (3.5%) and strength (9%), with activation of catabolic signaling pathways . In addition, disuse periods are accompanied by a loss of bone mineral density (BMD)  and an impaired cardiovascular capacity, with a loss in maximal oxygen consumption (VO2max) and cardiac output of 0.99% and 1.6% per day, respectively, during the first 2 weeks of bed rest .
Given the aforementioned deleterious effects of disuse situations, implementation of interventions aiming at accelerating the rate of healing and shortening the time needed before returning to competition is a major issue in sports. In this respect, several biological mechanisms underlying disuse-related muscle wasting might be involved (e.g., mitochondrial dysfunction with subsequent increased oxidative stress, reduction in myogenic capacity, systemic inflammation) and some remain to be elucidated, with muscle wasting ultimately resulting from an imbalance between muscle protein synthesis (MPS) and breakdown (MPB) . Specifically, decreases in MPS seem to be the main determinants of muscle wasting during disuse situations . In this respect, dietary protein intake is a powerful stimulus for MPS promotion , and for this reason, nutritional strategies (notably amino acid/protein supplementation and use of antioxidant compounds or anti-inflammatory drugs) have been a focus of attention for attenuating muscle wasting during disuse situations [50, 79, 84, 85]. However, the importance of physical strategies is often disregarded.
Blood Flow Restriction and Vascular Occlusion
Although controversy exists , one of the processes that is thought to facilitate hypertrophy is metabolic stress , which can be induced by resistance exercise training (RET) to failure but also by other strategies such as blood flow restriction (BFR) . BFR is usually accomplished by inflating a cuff around the proximal part of the target limb to a pressure that blocks venous blood return without concomitantly blocking arterial inflow into the muscle [45, 46, 47]. BFR induces an increased release in growth hormone and insulin-like growth factor 1 (IGF-1), as a consequence of metabolite and H+ accumulation [35, 75], thereby facilitating anabolic processes and stimulating MPS [23, 86]. In addition, BFR elicits an increase in heat shock protein-72 , which can protect proteins from stress-induced injury . Therefore, BFR may be considered for the prevention of disuse-induced muscle atrophy, with meta-analytic evidence in fact supporting its effectiveness for increasing muscle mass and strength in the general population [45, 46, 47, 70] and in the rehabilitation field .
Two daily sessions of BFR alone (i.e., with no exercise) with a pressure high enough to elicit arterial occlusion (i.e., five repetitions of 5 min duration with a cuff pressure of 238 mmHg separated by a 3 min-recovery without occlusion) for 2 weeks have proven effective in attenuating the reduction in quadriceps cross-sectional area in subjects who could not exercise due to knee immobilization following ACL reconstruction surgery . A similar BFR protocol proved to be even more effective than isometric RET for preventing loss of muscle mass and strength in subjects who had a casted knee for 2 weeks , although no benefits have been found in muscle mass with a restriction pressure below 50 mmHg . Therefore, although there is still some controversy, high levels of BFR (~ 200 mmHg) might be an effective passive strategy for the prevention of disuse-induced muscle mass when volitional exercise is not feasible.
Importantly, BFR seems especially useful in increasing muscle mass and strength when applied simultaneously with low-intensity physical exercise (also known as “KAATSU” training) which is sometimes feasible during the first stages of the recovery from an injury [45, 46, 47]. A recent study found increases in MPS rates and activation of anabolic signaling pathways when BFR (up to 200 mmHg) was applied in healthy subjects simultaneously with exercise but not when applied under resting conditions . As this study was conducted in healthy individuals, further research should address if the application of BFR under resting conditions can stimulate MPS in other populations (e.g., disuse situations, injured athletes). Walking twice a day for a duration of 10 min while BFR is applied to the lower limbs is sufficient to induce muscle hypertrophy  and to increase markers of bone anabolism  in young healthy men. Moreover, performing low volume endurance exercise (15 min at 40% of maximum oxygen uptake [VO2max]) concomitantly with BFR elicits greater benefits in muscle mass and strength than 45 min of the same exercise without BFR . Low-intensity exercise training during BFR is also an effective tool in the rehabilitation context as confirmed by a recent meta-analysis of 20 studies . For instance, low-load RET in combination with BFR has been proven to accelerate the recovery of muscle mass in subjects submitted to ACL reconstruction , although some conflicting results have been reported in athletes . Cook et al.  showed that the combination of BFR together with low-intensity RET prevented loss of muscle mass and strength in healthy subjects during a 30-day period of unilateral lower limb suspension. Other authors showed that the effects on muscle mass and strength of applying BFR simultaneously with low-intensity RET during a rehabilitation programme were similar to those elicited by high-intensity RET alone .
On the other hand, in order to ensure safety without compromising intervention efficacy, some methodological issues should be considered . Notably, BFR pressure should not surpass 80% of the arterial occlusion pressure . In this regard, targeting a score of 7 on a perceived pressure scale ranging from 0 to 10 (with 10 indicating most intense pressure) has been proposed as a more practical and feasible (albeit less accurate) option . Wider cuffs (i.e., 6–13.5 cm), which allow the achievement of occlusion at lower pressures, are recommended for the legs whereas 3–6 cm is the recommended range for the arms . Furthermore, to maximize adaptations it would be advisable to perform a progression of the stimulus from the application of BFR alone during bed rest or total inactivity to its use simultaneously with light endurance exercise or low-load RET (i.e., at 20–40% of one-repetition maximum) [45, 46, 47, 67].
Neuromuscular Electrical Stimulation
Neuromuscular electrical stimulation (NMES) is the transcutaneous application of electrical currents to a muscle group thereby depolarizing motor neurons and resulting in actual muscle contraction . Because this modality can generate involuntary muscle tension, it is frequently used as a passive surrogate of active training in several populations. NMES has been proposed as effective in the sport context [26, 27, 49, 62], and it could also be beneficial for clinical populations . Indeed, NMES acts as an “exercise simulator”. On the one hand, low-frequency NMES can activate the same signaling pathway as endurance exercise (notably, peroxisome proliferator-activated receptor gamma coactivator 1-alpha [PGC-1α]). In turn, high-frequency NMES activates the same signaling pathways as RET (i.e., mammalian target of rapamycin [mTOR], which promotes the activation of insulin and IGF-1 receptors) . NMES has also proven to activate the same corticomotor pathways as voluntary exercise [9, 22]. Moreover, it induces a synchronic motor unit recruitment that is independent of muscle fiber type, and thus high loads are not needed to recruit type II muscle fibers . For these reasons, this technique could be especially useful for populations with difficulties in performing exercise (e.g., during the first stages of recovery from injury) [11, 17, 84].
NMES has been proven to be effective for preventing the reduction of MPS, muscle mass and strength after ACL injury [15, 24, 78]. NMES also attenuates loss of oxidative enzymatic activity and leg muscle mass/strength in subjects submitted to 30 days of bed rest . Dirks et al.  found that NMES increased MPS and inhibited the activation of protein degradation pathways in subjects with knee immobilization for 5 days, thereby preventing muscle mass loss . In addition, NMES increases muscular and functional resistance especially in clinical patients , as well as muscle oxidative capacity  and VO2max [44, 80]. In addition, similar to endurance training, NMES increases antioxidant capacity [26, 27], therefore proving useful in reducing the redox imbalance elicited by disuse periods .
On the other hand, some authors have reported benefits at the neural level after NMES [26, 27, 28]. Yet, whether these benefits are translated into dynamic actions remains unclear [26, 27]. In this respect, although NMES is usually administered passively, it can also be applied simultaneously with (or “superimposed onto”) voluntary physical exercise (i.e., eliciting electrically-evoked contractions at the same time that the patient performs voluntary exercise). The rationale for applying NMES superimposed onto exercise is based on the hypothesis that, owing to the synchronic recruitment pattern of NMES, more motor units would be recruited than with voluntary exercise alone. Although there is controversy regarding the additional benefits of “superimposed” NMES in trained subjects vs voluntary exercise alone, the former could be effective in untrained subjects or in patients . Notably, superimposed NMES seems more effective than voluntary exercise alone for the prevention of muscle atrophy, muscle oxidative capacity and strength loss and for the recovery of knee functionality and gait kinematics after ligament surgery [20, 71]. However, a previous study found that voluntary exercise is at least as beneficial as superimposed NMES, although the latter could produce additional benefits in weaker muscles .
Regarding methodological recommendations for NMES sessions—which typically last ~ 30 to 60 min—stimulation frequency and pulse (biphasic rectangular pulses) duration should range between 50–75 Hz and 100–400 µs, respectively, and the intensity applied should be the highest tolerable to maximize force production . Sessions should be every day or even several times a day in patients with marked activation deficits (e.g., early after knee surgery), but a low-volume high-intensity approach (i.e., alternate days) should be adopted to target muscle hypertrophy once neural deficits are improved .
The potential of a vibratory stimulus (whether applied locally or to the whole body using a platform) to increase muscle mass and performance in healthy subjects has been previously discussed . Previous animal studies applying isolated vibration have reported benefits at the muscle level [21, 37, 74]. Yet, the potential benefits of vibration per se (i.e., independently of RET) on human muscle mass remain to be clearly shown. By contrast, due to the influence of mechanical stimuli on bone anabolism  and to the effectiveness of vibration to evoke an involuntary muscle contraction through the activation of stretch reflexes [3, 21], this technique could be potentially useful to mitigate the bone loss associated with immobilization.
The local application of vibration alone can induce significant benefits at the muscular level in populations at risk of muscle atrophy, such as the elderly [59, 77], and there is growing evidence that it can also provide some benefits in young healthy subjects by increasing muscle strength and cortical voluntary activation in the long-term [43, 72, 73]. Moreover, it seems to be effective in preventing bone degeneration associated with disuse situations. In subjects submitted to 90 days of bed rest, 10 min of vibration daily was sufficient to diminish or even circumvent the negative changes at the spinal level associated with immobilization (i.e., increased spinal length, intra-vertebral disc expansion and changes in disc convexity), also reducing the prevalence of back pain . However, the effects on back intrinsic muscle mass did not reach statistical significance. Similarly, Zange et al.  did not report benefits on muscle mass after applying a vibratory stimulus twice daily (5 min per session) during 2 weeks of bed rest .
On the other hand, the combination of vibration and RET can provide several benefits during disuse situations, including an attenuation in the loss of muscle/mass strength or bone mass . However, because most studies have applied both stimuli synchronously, it is not possible to discern the beneficial effect of the vibratory stimulus per se. Previous research has analyzed whether the combination of vibration together with RET during immobilization periods could provide benefits beyond those provided by RET alone. In subjects submitted to 60 days of bed rest, a vibration stimulus superimposed onto RET proved as effective for the reduction of muscle atrophy, pain and muscle damage as RET alone . However, another study found that ‘superimposed’ vibration provided additional benefits in the reduction of the bone loss during the same immobilization model .
Regarding methodological recommendations, there is no clear evidence supporting the optimal vibration protocol. However, it has been recently proposed that a vibratory stimulus with a frequency of 50–120 Hz and an amplitude of 1 mm should be applied to the tendon—rather than the muscle—to optimize the effects of local vibration . By contrast, when using whole body vibration, most studies have used frequencies ranging from 20 to 45 Hz  with some evidence supporting the fact that greater myoelectric activity could be achieved with higher frequencies (60 Hz) and amplitudes (4 mm) . Frequencies around or below 5 Hz should be avoided to prevent excessive resonance and caution should be taken with frequencies below 20 Hz .
Conclusions and Future Perspectives
The recovery from a sports injury is frequently associated with a period of muscle inactivity or unloading. These situations elicit important deleterious adaptations in the organism at different levels (i.e., metabolic, anthropometric, muscular, cardiovascular and functional) and therefore interventions aimed at increasing the rate of healing and shortening the time needed before returning to normal training and competition is a major issue in sport.
Voluntary physical activity is the most effective intervention for preventing or at least attenuating disuse-induced adverse effects, but it might not be feasible during periods of forced bed rest or limb immobilization. In this respect, several passive strategies might be applied. BFR alone or applied simultaneously with low-intensity exercise has demonstrated promising results for preventing disuse-induced muscle atrophy. The involuntary muscle contractions elicited by NMES training can also reduce the loss of muscle mass, force and oxidative capacity associated with disuse periods. Lastly, the mechanical stimulus elicited by vibration seems effective in reducing the loss of BMD that accompanies these situations and could also provide some benefits at the muscle level. Notwithstanding, it would be advisable to perform a progression of the applied stimuli and ultimately apply these strategies in conjunction with voluntary exercise.
This work is supported by the University of Alcalá (contract number FPI2016 to Valenzuela); the Spanish Ministry of Education, Culture and Sport (contract number FPU14/03435 to Morales); and the Spanish Ministry of Economy and Competitiveness (Fondo de Investigaciones Sanitarias and Fondos FEDER, grant numbers PI15/00558 and PI18/00139 to Lucia).
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
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