FES-rowing attenuates bone loss following spinal cord injury as assessed by HR-pQCT

Abstract

Neurologically motor complete spinal cord injury (SCI) presents a unique model of bone loss whereby specific regional sites are exposed to a complete loss of voluntary muscle-induced skeletal loading against gravity. This results in a high rate of bone loss, especially in the lower limbs where trabecular bone mass decreases by ~ 50-60% and cortical bone mass decreases by 25-34% before the rate of bone loss slows. These SCI-induced losses that are likely superimposed on continual age-related bone losses, increase the risk of low-impact fragility fracture. The fracture incidence 20 years post SCI is reported to be 4.6% per year. An intervention that effectively prevents, attenuates, or reverses bone loss is therefore highly desirable. We present a case study of an individual with chronic complete SCI, where bone loss has been attenuated following long-term functional electrical stimulation (FES)-rowing training. In this case study, we characterize the ultradistal tibia and ultradistal radius of the FES-rower with chronic complete SCI using high-resolution-peripheral quantitative computed tomography. These data are compared with a group of FES-untrained individuals with chronic complete SCI and to a normative non-SCI cohort. The evidence suggests, albeit from a single individual, that long-term FES-rowing training can attenuate bone loss secondary to chronic complete SCI. Indeed, key FES-rower's bone metrics for the ultradistal tibia more closely resemble normative age-matched values, which may have clinical significance since the majority of fragility fractures in chronic SCI occur in the lower extremities. Neurologically motor complete spinal cord injury (SCI) presents a unique model of bone loss whereby specific regional sites are exposed to a complete loss of voluntary muscle-induced skeletal loading against gravity. The initial loss of bone mineral content is estimated to approach 4% per month in trabecular sites, and 2% per month in cortical sites. 1 Trabecular bone mass is estimated to decrease by 48% of pre-injury values in the femur, reaching a new slower rate of loss by 3 years and 58% in the tibia by 5 years. Cortical bone mass decreases by 34% of pre-injury values in the femur by 5 years, and 25% in the tibia by 7 years. 2 These losses are likely superimposed on continual age-related bone loss. 3 SCI-induced bone loss often leads to the development of osteoporo-sis, which increases the risk of low-impact fragility fracture. 4 The fracture incidence 20 years post SCI is reported to be 4.6% per year. 5 Thus, even active individuals with complete SCI at age 20 undergoing conventional standard of care have a very high likelihood of sustaining a fragility fracture in their lifetime, markedly affecting quality of life and increasing the risk of mortality. 6 An intervention that effectively prevents, attenuates or reverses bone loss is therefore highly desirable. 7 One such intervention under investigation is functional electrical stimulation (FES) rowing. 8 In the present configuration, FES-rowing is an exercise that combines voluntary upper-limb concurrent with FES-assisted lower-limb exercise involving the quadriceps, hamstrings, tibialis anterior and triceps surae musculature. The training program, which involves three 30-min FES-rowing sessions and four 60-min FES-activated knee extension exercise sessions per week, has been previously described in detail. 9 FES-rowing is well tolerated by males and females with complete and incomplete injury between C4 (with a zone of partial preservation that permits a level of elbow flexion) and T12. In addition, there have been no reported medical complications related to FES-rowing training. Furthermore, any increased spasticity is managed by daily FES-training without the need for anti-spasmodic medications. Gibbons et al. 8 recently reported the potential to modulate bone loss in a male, age of 59 years with a T4 complete SCI following a road traffic accident, who is highly trained (412 years) in FES-rowing. The individual was 14 years post injury, with no history of musculoskeletal complications or medications known to affect bone (calcium, vitamin D or antiresorptive drugs). Although lower limb spasticity has increased since this individual's injury, daily FES-assisted exercise and passive standing successfully manages the condition without the need for anti-spasmodic medications. In Gibbons et al. 8 bilateral trabecular bone density in the proximal tibia was reported using peripheral quantitative computed tomography (Stratec XCT3000, Pforzheim, Germany). The FES-rower's bone metrics were compared with data from a previous study involving a non-SCI cohort (n = 14; mean age of 37 years) and a cohort of chronic SCI who were FES-untrained (n = 9; mean age of 32 years; mean of 6.6 years post injury). 10 Compared with the non-SCI cohort, the FES-rower had mean proximal tibia bone density in the non-dominant limb that was 0.57 s.d. lower, which is considered within the normal range based on the criterion of no more than 1.0 s.d. lower than the general population mean. The chronic SCI cohort had an average bone density that was 1.66 s.d. lower than the mean for non-SCI individuals. However, key limitations of that study include the lack of age-matched normative data, the relatively small number of