High-volume FES-cycling partially reverses bone loss in people with chronic spinal cord injury
Introduction
Complete spinal cord injury (SCI) leads to an extreme form of immobilisation in the paralysed limbs. As a consequence, a marked and rapid atrophy of the vascular system [41] and muscle tissue [1], [8], [13], and a loss of bone tissue in the paralysed regions [3], [14], [15], [21], [32] manifests itself. Within the first few years after SCI, bone mineral content (BMC) decreases by around 45% in the femur [18], [34] and by 56% in the tibia [18]. More specifically, the most affected bone sites are the cancellous compartments of the long bones [3], [14], [18], [34], leading to a mean deficit of 73% in trabecular bone mineral density (BMD) in the distal tibia compared to able-bodied values [18]. Secondary to this bone loss, fractures caused by minimal trauma often occur in the paralysed lower extremities. The skeletal sites most prone to fractures are the distal femur and the proximal and distal tibia [17], [26], [35], [44], with an estimated fracture incidence of twice the incidence in able-bodied people [50], [51].
It is still unknown whether unloading of the bones in the paralysed extremities is the only factor causing the rapid sublesional bone loss or if other factors such as neuronal, humoral and vascular adaptations after a spinal lesion are also involved [9], [39], [47], [48], [49]. Several studies have shown that there is no bone loss in the upper extremities of persons with paraplegia [3], [15], [18], [21], disproving the hypothesis that bone loss following SCI is systemic. Rather, local unloading of the bones in the paralysed extremities together with the detrimental effects of SCI on muscle tissue and the vascular and neuronal systems are the major factors responsible for the rapid and vast bone loss after SCI, as postulated by Frost's mechanostat theory many years earlier [22], [23], [24], [25].
Previous studies investigated the effect of reloading the leg bones via muscle contractions induced by functional electrical stimulation (FES) using exercise modalities such as cycling [2], [4], [10], [16], [29], [36], [37], [42]. The findings of the impact of FES-cycle training on the bones of the paralysed limbs were equivocal: some found no bone adaptations [2], [16], [36], [42] while others documented a reduction in the rate of bone loss [29] or even a recovery of BMD [4], [10], [37]. In most of these studies, training volume was set at 3 sessions per week during six [16], [29], [36], nine [4] or twelve months [37]. In contrast, Chen et al. [10] investigated the effect of a more intensive FES-cycle training regime of 30 min, five times per week, at a sub-maximal resistance load, over a period of six months. They found a recovery in areal BMD of 11.1% in the distal femur and of 12.9% in the proximal tibia in people with chronic complete SCI. Similarly, Mohr et al. [37] conducted a less intensive FES-cycle training programme (three weekly sessions) but for a longer duration (12 months), and found a comparable increase in areal BMD of 10% in the proximal tibia.
In summary, these results suggest a potentially positive and site-specific effect of FES-induced exercise on bones after SCI. Because the cited studies on FES-cycling indicate that there may be a dose-dependent effect, the present study investigated the effect of high-volume FES-induced cycle training on the leg bones in subjects with long-lasting and complete SCI. In contrast to other groups who investigated the osteogenic effect of an FES-cycle training programme by means of dual energy X-ray absorptiometry (DXA), we performed peripheral quantitative computed tomography (pQCT) scans at several sites in the femur and tibia in order to achieve the most detailed assessment to date with regard to volumetric BMD and bone geometry. In addition, to determine the time course of the osteogenic effect, bone and soft tissue parameters in the lower limbs were assessed three times: before, during and after the FES-training programme.
Section snippets
Methods
This study was conducted as a multi-centre trial at: 1) the Queen Elizabeth National Spinal Injuries Unit and the University of Glasgow, Glasgow, United Kingdom; 2) Division of Applied Biomedical Research, King's College London, London, United Kingdom; and 3) Swiss Paraplegic Research, Nottwil, Switzerland. The study was approved by the Ethics Committees of King's College Hospital and King's College London, the Southern General Hospital in Glasgow and the Canton of Lucerne.
Subjects
A total of 12 SCI subjects were recruited at the three centres: three at the Queen Elizabeth National Spinal Injuries Unit, five at the Division of Applied Biomedical Research, Kings College London and four at Swiss Paraplegic Research. All subjects fulfilled the following inclusion criteria: motor-complete post-traumatic medullary lesion between T3 and T12 (grade A on the American Spinal Injuries Association (ASIA) impairment scale), at least three years post injury, and greater than 18 years
Muscle conditioning
In order to prepare the paralysed muscles for the FES-cycle training, the subjects first performed muscle conditioning training. For the muscle conditioning, we used an 8-channel-stimulator (Stanmore Stimulator) with the following stimulation parameters: pulse frequency of 50 Hz, pulse width of 300–400 µs, an amplitude between 80 and 150 mA and a 1:1 duty cycle set at 6 s on/off. The training consisted of 30 to 60 min of isometric bilateral FES three to five times weekly, with surface
Study subjects
One subject had to terminate the study due to a foot fracture which occurred seven months into the study, but which was unrelated to the FES-cycle training. Subject characteristics of the remaining eleven subjects are shown in Table 1.
Muscle conditioning
To prepare muscles in the paralysed legs for FES-cycling, subjects performed on average 14 ± 7 weeks (range 6 to 32 weeks) of muscle conditioning.
FES-training compliance
Overall, subjects completed an average of 79.3% of the scheduled FES-cycle training sessions, corresponding to 3.7 ± 0.6
Discussion
This study is the first to investigate the impact of a high-volume FES-cycle training programme on bone parameters in the lower extremities of subjects with chronic complete SCI, by means of pQCT. After 19.0 ± 2.1 months FES exercise (i.e. initial muscle conditioning followed by high-volume FES-cycle training) the bone parameters of the femur had changed significantly. In the distal femur BMDtrab increased by approximately 14% and BMDtot by 7%. In contrast, decreases of less than 2% were found in
Conclusion
High-volume FES-cycling induces site-specific bone adaptation in the paralysed limbs of persons with long-lasting SCI. This is the first study that has assessed the effect of high-volume FES-cycling in this population at several measurement sites of the legs, using pQCT. The detailed study of various sites in the legs revealed that bone formation is limited to the distal femur. Bone formation may also occur in the shaft of the femur, but observation times longer than in the present study would
Acknowledgments
We gratefully acknowledge all subjects that participated in the study for dedicating their time and effort. We also thank Dr Lynsey Duffell and Ms Helen Berry for their helpful contribution to the study and Dr Ben Saunders and Mr Pius Hofer for their excellent technical support. We would also like to thank Ms Helen Berry, for permission to use the peak power output data. This work was supported by the Engineering and Physical Sciences Research Council (grants GR/R93520, London and GR/R92462,
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