Objective: To investigate adaptive changes in bone and muscle parameters in the paralysed limbs after de-training or reduced functional electrical stimulation (FES) induced cycling following high-volume FES-cycling in chronic spinal cord injury (SCI). 

Subjects: Five subjects with motor-sensory complete SCI (age 38.6 years, lesion duration 11.4 years) were included. Four subjects stopped FES-cycling completely after the training phase whereas one continued reduced FES-cycling (2-3 times/week, for 30min).

Methods: Bone and muscle parameters were assessed in the legs using peripheral quantitative computed tomography at six and twelve months after cessation of high-volume FES-cycling. 

Results: Gains achieved in the distal femur by high-volume FES-cycling were partly maintained at one year of detraining: 73.0% in trabecular bone mineral density (BMD), 63.8% in total BMD, 59.4% in bone mineral content and 22.1% in muscle cross-sectional area (CSAmuscle) in the thigh. The subject who continued reduced FES-cycling maintained 96.2% and 95.0% of the previous gain in total and trabecu-lar BMD, and 98.5% in CSAmuscle. 

Conclusion: Bone and muscle benefits achieved by one year of high-volume FES-cycling are partly preserved after 12 months of detraining whereas reduced cycling maintains bone and muscle mass gained. This suggests that high-volume FES-cycling has clinical relevance for at least 1y after detraining

Coupaud, S.

Eser, P.

Frotzler, A.

Hunt, K.J.

Kakebeeke, T.H.

Perret, C.

English

To investigate adaptive changes in bone and muscle parameters in the paralysed limbs after detraining or reduced functional electrical stimulation (FES) induced cycling following high-volume FES-cycling in chronic spinal cord injury. Five subjects with motor-sensory complete spinal cord injury (age 38.6 years, lesion duration 11.4 years) were included. Four subjects stopped FES-cycling completely after the training phase whereas one continued reduced FES-cycling (2–3 times/week, for 30 min). Bone and muscle parameters were assessed in the legs using peripheral quantitative computed tomography at 6 and 12 months after cessation of high-volume FES-cycling. Gains achieved in the distal femur by high-volume FES-cycling were partly maintained at one year of detraining: 73.0% in trabecular bone mineral density, 63.8% in total bone mineral density, 59.4% in bone mineral content and 22.1% in muscle cross-sectional area in the thigh. The subject who continued reduced FES-cycling maintained 96.2% and 95.0% of the previous gain in total and trabecular bone mineral density, and 98.5% in muscle cross-sectional area. Bone and muscle benefits achieved by one year of high-volume FES-cycling are partly preserved after 12 months of detraining, whereas reduced cycling maintains bone and muscle mass gained. This suggests that high-¬volume FES-cycling has clinical relevance for at least one year after detraining

Frotzler, Angela

Coupaud, Sylvie

Perret, Claudio

Kakebeeke, Tanja

Hunt, Kenneth

Eser, Prisca

University of Strathclyde Institutional Repository

Strathprints Institutional RepositoryFrotzler, Angela and Coupaud, Sylvie and Perret, Claudio and Kakebeeke, Tanja and Hunt, Kennethand Eser, Prisca (2009) Effect of detraining on bone strength in subjects with chronic spinal cordinjury after a period of electrically-stimulated-cycling : a small cohort study. Journal of RehabilitationMedicine, 41 (4). pp. 282-285. ISSN 1650-1977Strathprints is designed to allow users to access the research output of the University of Strathclyde.Copyright c© and Moral Rights for the papers on this site are retained by the individual authorsand/or other copyright owners. You may not engage in further distribution of the material for anyprofitmaking activities or any commercial gain. You may freely distribute both the url (http://strathprints.strath.ac.uk/) and the content of this paper for research or study, educational, ornot-for-profit purposes without prior permission or charge.Any correspondence concerning this service should be sent to Strathprints administrator:mailto:strathprints@strath.ac.ukhttp://strathprints.strath.ac.uk/J Rehabil Med 41ORIGINAL REPORTJ Rehabil Med 2009; 41: 282–285© 2009 The Authors. doi: 10.2340/16501977-0321Journal Compilation © 2009 Foundation of Rehabilitation Information. ISSN 1650-1977Objective: To investigate adaptive changes in bone and muscle parameters in the paralysed limbs after detraining or reduced functional electrical stimulation (FES) induced cycling following high-volume FES-cycling in chronic spinal cord injury. Subjects: Five subjects with motor-sensory complete spinal cord injury (age 38.6 years, lesion duration 11.4 years) were included. Four subjects stopped FES-cycling completely after the training phase whereas one continued reduced FES-cycling (2–3 times/week, for 30 min).Methods: Bone and muscle parameters were assessed in the legs using peripheral quantitative computed tomography at 6 and 12 months after cessation of high-volume FES-cycling. Results: Gains achieved in the distal femur by high-volume FES-cycling were partly maintained at one year of detrain-ing: 73.0% in trabecular bone mineral density, 63.8% in to-tal bone mineral density, 59.4% in bone mineral content and 22.1% in muscle cross-sectional area in the thigh. The sub-ject who continued reduced FES-cycling maintained 96.2% and 95.0% of the previous gain in total and trabecular bone mineral density, and 98.5% in muscle cross-sectional area. Conclusion: Bone and muscle benefits achieved by one year of high-volume FES-cycling are partly preserved after 12 months of detraining, whereas reduced cycling maintains bone and muscle mass gained. This suggests that high- volume FES-cycling has clinical relevance for at least one year after detraining. Key words: bone loss, detraining, functional electrical stimula-tion, osteoporosis, spinal cord injury.J Rehabil Med 2009; 41: 282–285Correspondence address: Sylvie Coupaud, Centre for Reha-bilitation Engineering, Department of Mechanical Engineer-ing, University of Glasgow, Glasgow G12 8QQ, UK. E-mail: s.coupaud@mech.gla.ac.uk Submitted July 14, 2008; accepted October 10, 2008INTRODUCTIONSpinal cord injury (SCI) leads to a rapid and distinct reduction in bone tissue in the paralysed regions (1). The most affected areas are the metaphyseal-epiphyseal regions of the distal femur, and of both the proximal and distal tibia, where bone mineral content (BMC) is reduced by approximately 50% and 70%, respectively, within the first few years post-injury (2). The clinical significance of this bone loss and associated reduction in bone strength is that it exposes those with SCI to a high risk of low-energy fractures, with a lifetime risk of suffering a fracture in the lower limbs being twice as high as in able-bodied people (3). In order to increase bone strength in the paralysed limbs and reduce fracture risk, the application of load on bones in people with SCI was investigated. Active loading i.e. through muscle contractions by means of functional electrical stimula-tion (FES)-induced cycling was found to lead to a site-specific recovery in bone mineral density (BMD) in the paralysed legs up to 14% (4–6). However, despite the positive effect of FES-cycling on bones after SCI, little is known about bone behaviour in the paralysed limbs once the FES-cycling is discontinued. To our knowledge only 2 groups (4, 5) have as yet investigated the impact of a reduced FES-cycle training programme or detraining on bone status in the paralysed limbs. Both groups found that the partially reversed bone loss after initial FES-cycling was lost within the subsequent 6 months of either reduced FES-cycling or detraining. However, whether an initial phase of high-volume FES-cycling causes similar bone adaptations during detraining or reduced FES-cycling remains unclear.The aim of the present study was therefore to investigate the impact of detraining or reduced FES-cycling following a one-year high-volume FES-cycle training on bones and soft tissue in the paralysed limbs of people with chronic complete SCI by detailed peripheral quantitative computed tomography (pQCT) assessment. For this purpose, we performed a follow-up study of the subjects who participated in the previously published study on the osteogenic effects of high-volume FES-cycling (6). MATERIALS AND METHODSThe study was conducted as a multi-centre design at the Queen Elizabeth National Spinal Injuries Unit and the University of Glasgow, Glasgow, UK as well as at the Swiss Paraplegic Research, Nottwil, Switzerland. The study was approved by the local ethics committees. EFFECT OF DETRAINING ON BONE AND MUSCLE TISSUE IN SUBJECTS WITH CHRONIC SPINAL CORD INJURY AFTER A PERIOD OF ELECTRICALLY-STIMULATED CYCLING: A SMALL COHORT STUDYAngela Frotzler, PhD1, Sylvie Coupaud, PhD2,3, Claudio Perret, PhD1, Tanja H. Kakebeeke, PhD1, Kenneth J. Hunt PhD2,3 and Prisca Eser, PhD4From the 1Swiss Paraplegic Research, Nottwil, Switzerland, 2University of Glasgow, and 3Queen Elizabeth National Spinal Injuries Unit, Glasgow, UK and the 4Department of Rheumatology and Clinical  Immunology/Allergology, University Hospital Bern, Bern, Switzerland283Bone and muscle parameters after FES-cycling in SCI SubjectsEleven people with a chronic SCI participated in a high-volume FES-cycling programme (up to 5 sessions per week, for one year) as published previously (6). Of those, 4 men and one woman aged 38.6 (standard deviation (SD) 8.1) years (age range 27.7–48.4 years) who showed a significant training effect on bone parameters attended follow-up investigations after termination of the high-volume FES-cycling programme. All subjects had motor-complete post-traumatic paraplegia (grade AIS A, i.e. American Spinal Injury Association (ASIA) impairment scale (AIS) (7)), with a lesion level between T4 and T7 and a lesion duration of 11.4 (SD 7.0) years (range 3.6–19.8 years). Exclusion criteria were current or past unhealed bone fractures, diseases known to affect bone metabolism and use of bone acting drugs. All subjects were informed about the protocol for the bone measuring procedure and were required to sign an informed consent form. Reduced FES-cycle training or detraining At the end of the 12-month high-volume FES-cycling programme (for more training details see Frotzler et al. (6)), subjects were free to stop or continue the FES-cycling at their own desired training volume (as determined by the number and duration of sessions per week and the training intensity, i.e. resistance). Four subjects stopped the FES-cycling programme and one subject decided to continue a reduced FES-cycle training and performed 2–3 training sessions per week, each lasting 30 min.MeasurementsBone and soft tissue measurements were performed with a pQCT scan-ner (model XCT 3000, Stratec Medical, Pforzheim, Germany) with regard to volumetric BMD and bone geometry, as well as muscle and fat cross-sectional areas. Image processing and calculation of numeri-cal values were performed using the manufacturer’s software package (version 6.0 B). Peripheral QCT scans were performed 4 times: at baseline prior to the FES-intervention (t1), at the end of the high- volume FES-cycling programme (t2), as well as after 6 (t3) and 12 months (t4) of detraining or reduced training. Bone data at t1 and t2 have been published previously (6). In the tibial and femoral epiphyses, BMC, total BMD (BMDtot) and trabecular BMD (BMDtrab) were calculated. In the diaphyses, BMC and cortical BMD (BMDcort) were calculated. In addition, muscle cross-sectional area (CSAmuscle) and fat CSA (CSAfat) both in the thigh and the shank were also identified. Statistical analysisDue to the small number of subjects, only descriptive statistics were performed. The mean and SD of the changes in bone and soft tissue parameters between t2 and t3, and between t3 and t4 were calculated to analyse the impact of detraining or reduced FES-cycling. To describe the effect of detraining or reduced FES-cycling, changes in bone and soft tissue parameters between t1 and t2 were compared with those between t2 and t4.RESULTSImpact of detraining on bone and soft tissue Within 12 months of detraining, a mean of 73.0% (SD 13.4) of the total bone gain achieved between t1 and t2 in BMDtrab in the distal femur was still preserved at t4 (Fig. 1). At this site, 63.8% (SD 8.0) gained in BMDtot and 59.4% (SD 3.9) gained in BMC during the FES-cycling period were also preserved at t4. In the femoral shaft, BMC and BMDcort decreased by 1.8% (SD 0.8) and 3.6% (SD 2.8) between t2 and t4, which is comparable to the decreases in this site found between t1 and t2. With regard to the impact of detraining on soft tissue in the thigh, 22.1% (SD 21.0) of the total increase in CSAmuscle achieved between t1 and t2 was preserved after 12 months of detraining. The main decrease of the total gain in CSAmuscle (68.6% (SD 34.0)) occurred within the first 6 months of detraining, i.e. between t2 and t3. CSAfat in the thigh did not change considerably during the FES-cycling programme, but increased in the phase of de-training and was, on average, 7.6% higher at t4 than at t1. With regard to the impact of detraining on the tibia, bone parameters at this site only changed by between –1.3% and 1.6%. This is similar to the negligible bone changes found during the high-volume FES-cycling programme between t1 and t2. Soft tissue parameters in the lower leg also showed only minor changes between t2 and t4: both CSAmuscle and CSAfat increased on average by 3.2% and 3.5%. Impact of reduced FES-cycling on bone and soft tissue One subject continued a reduced FES-cycle training programme between t2 and t4 and was able to preserve 96.2% and 95.0% of the total gain in distal femoral BMDtot and distal femoral BMDtrab (Fig. 1) achieved during high-volume FES-cycling. In the femoral shaft, BMC and BMDcort decreased by 7.3% and 5.4%, respectively, between t2 and t4. It should be noted that BMC at this site showed similar decreases during high-volume FES-cycling, i.e. between t1 and t2. With regard to the impact of reduced FES-cycling on the soft tissue in the thigh, both CSAmuscle and CSAfat decreased by 1.5% and 17.0%. Thus, nearly the complete gain in muscle tissue achieved during high-volume FES-cycling was still preserved at t4. In the tibial epiphysis and diaphysis, bone parameters showed decreases of between 1.3% and 4.8% in the phase of reduced FES-cycling. Interestingly, these decreases are less pronounced than those observed in this subject during high-volume FES-cycling with decreases in tibial bone parameters of up to 18.6%. Fig. 1. Adaptive changes in trabecular bone mineral density (BMD) of the distal femur. Values are shown at baseline (t1), after 12 months of high-volume functional electrical stimulation (FES)-cycling (t2), and after 6 (t3) and 12 months (t4) of detraining or reduced FES-cycle training. Note that one subject (black line) continued reduced FES-cycling between t2 and t4, whilst 4 participants (grey lines) stopped high-volume FES-cycling at t2. The dashed line indicates the start of the detraining or reduced FES-cycling following high-volume FES-cycling.J Rehabil Med 41284 A. Frotzler et al.DISCUSSIONThe effect of detraining or reduced FES-cycle training fol-lowing 12 months of high-volume FES-cycling on bones in the lower extremities of 5 persons with chronic complete SCI was investigated. This is the first study with such a long FES-intervention and follow-up period and the first to measure bone and soft-tissue parameters by pQCT. Despite the small number of subjects the present study shows a clear tendency: between 59% and 73% of the gain achieved in BMC, BMDtot and BM-Dtrab in the distal femoral epiphysis following high-volume FES-cycling were still preserved after 12 months of detraining. This finding is in contrast to the documentations of Chen et al. (5), who found that after stopping FES-cycling (from 5 to zero FES-cycle training sessions per week) bone values returned to baseline levels within 6 months of detraining. According to our results, it appears to take more than 12 months of detraining to resorb the bone tissue that was gained within 12 months of high-volume FES-cycling. In addition, according to Wilmet et al. (8) who found a decrease of BMC of approximately 4% per month in areas rich in trabecular bone during the first year of SCI, bone loss following high-volume FES-cycling in people with chronic SCI seems to be slower with an average decrease in distal femoral BMC of 0.5% per month. The reason for this finding remains unclear, and needs to be investigated in further studies. We speculate that factors that affect bone metabolism, such as vascular atrophy after SCI, may slow down bone loss in people with chronic SCI. Regarding the muscle tissue in the paralysed legs, more than two-thirds of the muscle gain achieved during high-volume FES-cycling was lost within one year of detraining. This is comparable to the atrophy in CSAmuscle found in people after acute SCI (9). Reduced FES-cycle training (2.5 training sessions of 30 min per week) seemed to preserve the increase in both the bone at the distal femur and the muscle tissue of the thigh that resulted from high-volume FES-cycling. The present results are in contrast to the findings of Mohr et al. (4), who found the total gain in areal BMD (+10%) in the proximal tibia following FES-cycling for 30 min per day, 3 days per week for 12 months to be lost after a further 6 months with only one training session per week. It may be that there is an important difference between 1 and 2 training sessions per week, with one weekly training session turning a bone’s disuse mode “on”, thus resulting in resorption of the gained bone substance (as described by Frost (10)). According to Frost’s Mechanostat-theory (10), load-induced strains in bones provide the primary control signal underlying the biological responses of bone to its mechanical usage. Thus, strains above a certain threshold turn modelling “on”, resulting in an increased bone mass and strength. On the other hand, if strains are too small or absent, a disuse mode of remodelling turns “on” and bone will be resorbed until bone strength is adapted to its new mechanical usage. Consequently, one weekly training session may not be enough to preserve an adequate muscle mass necessary to induce large enough bone strains, while 2 sessions per week may preserve the previously achieved gain in muscle mass sufficiently in order to preserve the achieved gain in BMC. Several studies documented the fact that people with SCI are at a higher risk of low-trauma fractures (3), and that fractures mainly occur in the distal femur and in the distal and proximal tibia (11). Since fractures may lead to comorbidity and a reduc-tion in quality of life, improvement of bone parameters in the femur may have considerable clinical relevance. High-volume FES-cycling has the potential to increase bone strength of the distal femur in people with chronic and complete SCI (6). Hence, we assume that fracture risk at this site might be reduced after high-volume FES-cycle training and that this protective effect is subsequently sustained following a period of reduced FES-cycling, or even after 12 months of detraining. Indeed, the BMDtrab in the distal femur is reported to be the most sensi-tive bone parameter distinguishing between SCI persons with and without fractures (11). Four of our subjects had baseline BMDtrab values in the distal femur below the reported fracture threshold (11). However, at the end of the 30-month period of monitoring (including 12 months of high-volume FES-cycling and 12 months of detraining or reduced FES-cycling), all of our subjects, independent of whether they stopped or continued FES-cycling, remained above this fracture threshold. Thus, for a lasting improvement in bone parameters in the distal femur of people with chronic complete SCI we recommend a 2-phase FES-cycle training schedule, the first phase consisting of high-volume FES-cycle training in order to increase bone parameters, followed by the second phase consisting of reduced FES-cycle training in order to preserve bone parameters. Studies with even longer follow-up periods are needed to determine how long this second phase of reduced training volume may be.ACKNOWLEDGEMENTSWe gratefully acknowledge all subjects who participated in the study for dedicating their time and effort. This work was supported by the Engi-neering and Physical Sciences Research Council (grants GR/R92462, Glasgow) and the Swiss Paraplegic Foundation. REFERENCES1. Biering-Sorensen F, Bohr HH, Schaadt OP. Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury. Eur J Clin Invest 1990; 20: 330–335.2. Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, et al. Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 2004; 34: 869–880.3. Vestergaard P, Krogh K, Rejnmark L, Mosekilde L. Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord 1998; 36: 790–796.4. Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M. Increased bone mineral density after prolonged elec-trically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int 1997; 61: 22–25.5. Chen SC, Lai CH, Chan WP, Huang MH, Tsai HW, Chen JJ. Increases in bone mineral density after functional electrical stimu-lation cycling exercises in spinal cord injured patients. Disabil Rehabil 2005; 27: 1337–1341.6. Frotzler A, Coupaud S, Perret C, Kakebeeke TH, Hunt KJ, Donaldson N de N, et al. High-volume FES-cycling partially re-J Rehabil Med 41285Bone and muscle parameters after FES-cycling in SCI verses bone loss in people with chronic spinal cord injury. Bone 2008; 43: 169–176.7. Maynard FM Jr., Bracken MB, Creasey G, Ditunno JF Jr., Donovan WH, Ducker TB, et al. International Standards for Neurological and Functional Classification of Spinal Cord Injury. American Spinal Injury Association. Spinal Cord 1997; 35: 266–274.8. Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P. Longitudinal study of the bone mineral content and of soft tis-sue composition after spinal cord section. Paraplegia 1995; 33: 674–677.9. Castro MJ, Apple DF Jr., Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol 1999; 80: 373–378.10. Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec 1987; 219: 1–9.11. Eser P, Frotzler A, Zehnder Y, Denoth J. Fracture threshold in the femur and tibia of people with spinal cord injury as determined by peripheral quantitative computed tomography. Arch Phys Med Rehabil 2005; 86: 498–504.J Rehabil Med 41

Bone “mass” and the “mechanostat”: a proposal. Anat Rec

Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord

Fracture threshold in the femur and tibia of people with spinal cord injury as determined by peripheral quantitative computed tomography. Arch Phys Med Rehabil

High-volume FES-cycling partially reJ Rehabil Med 41 285Bone and muscle parameters after FES-cycling in SCI verses bone loss in people with chronic spinal cord injury.

High-volume FES-cycling partially reJ Rehabil Med 41285 Bone and muscle parameters after FES-cycling in SCI verses bone loss in people with chronic spinal cord injury.

Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int

Increases in bone mineral density after functional electrical stimulation cycling exercises in spinal cord injured patients. Disabil Rehabil

Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury.

International Standards for Neurological and Functional Classification of Spinal Cord Injury. American Spinal Injury Association. Spinal Cord

Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury.

Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia

Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals.

Effect of detraining on bone strength in subjects with chronic spinal cord injury after a period of electrically-stimulated-cycling : a small cohort study

Enlighten

      Frotzler, A. and Coupaud, S. and Perret, C. and Kakebeeke, T.H. and Hunt, K.J. and Eser, P. (2009) Effect of detraining on bone and muscle tissue in subjects with chronic spinal cord injury after a period of electrically-stimulated cycling: a small cohort study. Journal of Rehabilitation Medicine, 41(4). pp. 282-285. ISSN 1650-1977   http://eprints.gla.ac.uk/4938/  Deposited on: 24 March 2009   Enlighten – Research publications by members of the University of Glasgow http://eprints.gla.ac.uk ORIGINAL REPORTJ Rehabil Med 2009 PreviewJ Rehabil Med 41© 2009 The Authors. doi: 10.2340/16501977-0321Journal Compilation © 2009 Foundation of Rehabilitation Information. ISSN 1650-1977Objective: To investigate adaptive changes in bone and muscle parameters in the paralysed limbs after detraining or reduced functional electrical stimulation (FES) induced cycling following high-volume FES-cycling in chronic spinal cord injury. Subjects: Five subjects with motor-sensory complete spinal cord injury (age 38.6 years, lesion duration 11.4 years) were included. Four subjects stopped FES-cycling completely after the training phase whereas one continued reduced FES-cycling (2–3 times/week, for 30 min).Methods: Bone and muscle parameters were assessed in the legs using peripheral quantitative computed tomography at 6 and 12 months after cessation of high-volume FES-cycling. Results: Gains achieved in the distal femur by high-volume FES-cycling were partly maintained at one year of detrain-ing: 73.0% in trabecular bone mineral density, 63.8% in to-tal bone mineral density, 59.4% in bone mineral content and 22.1% in muscle cross-sectional area in the thigh. The sub-ject who continued reduced FES-cycling maintained 96.2% and 95.0% of the previous gain in total and trabecular bone mineral density, and 98.5% in muscle cross-sectional area. Conclusion: Bone and muscle benefits achieved by one year of high-volume FES-cycling are partly preserved after 12 months of detraining, whereas reduced cycling maintains bone and muscle mass gained. This suggests that high- volume FES-cycling has clinical relevance for at least one year after detraining. Key words: bone loss, detraining, functional electrical stimula-tion, osteoporosis, spinal cord injury.J Rehabil Med 2008; 00: 00–00Correspondence address: Sylvie Coupaud, Centre for Reha-bilitation Engineering, Department of Mechanical Engineer-ing, University of Glasgow, Glasgow G12 8QQ, UK. E-mail: s.coupaud@mech.gla.ac.uk Submitted July 14, 2008; accepted October 10, 2008INTRODUCTIONSpinal cord injury (SCI) leads to a rapid and distinct reduction in bone tissue in the paralysed regions (1). The most affected areas are the metaphyseal-epiphyseal regions of the distal femur, and of both the proximal and distal tibia, where bone mineral content (BMC) is reduced by approximately 50% and 70%, respectively, within the first few years post-injury (2). The clinical significance of this bone loss and associated reduction in bone strength is that it exposes those with SCI to a high risk of low-energy fractures, with a lifetime risk of suffering a fracture in the lower limbs being twice as high as in able-bodied people (3). In order to increase bone strength in the paralysed limbs and reduce fracture risk, the application of load on bones in people with SCI was investigated. Active loading i.e. through muscle contractions by means of functional electrical stimula-tion (FES)-induced cycling was found to lead to a site-specific recovery in bone mineral density (BMD) in the paralysed legs up to 14% (4–6). However, despite the positive effect of FES-cycling on bones after SCI, little is known about bone behaviour in the paralysed limbs once the FES-cycling is discontinued. To our knowledge only 2 groups (4, 5) have as yet investigated the impact of a reduced FES-cycle training programme or detraining on bone status in the paralysed limbs. Both groups found that the partially reversed bone loss after initial FES-cycling was lost within the subsequent 6 months of either reduced FES-cycling or detraining. However, whether an initial phase of high-volume FES-cycling causes similar bone adaptations during detraining or reduced FES-cycling remains unclear.The aim of the present study was therefore to investigate the impact of detraining or reduced FES-cycling following a one-year high-volume FES-cycle training on bones and soft tissue in the paralysed limbs of people with chronic complete SCI by detailed peripheral quantitative computed tomography (pQCT) assessment. For this purpose, we performed a follow-up study of the subjects who participated in the previously published study on the osteogenic effects of high-volume FES-cycling (6). MATERIALS AND METHODSThe study was conducted as a multi-centre design at the Queen Elizabeth National Spinal Injuries Unit and the University of Glasgow, Glasgow, UK as well as at the Swiss Paraplegic Research, Nottwil, Switzerland. The study was approved by the local ethics committees. EFFECT OF DETRAINING ON BONE AND MUSCLE TISSUE IN SUBJECTS WITH CHRONIC SPINAL CORD INJURY AFTER A PERIOD OF ELECTRICALLY-STIMULATED CYCLING: A SMALL COHORT STUDYAngela Frotzler, PhD1, Sylvie Coupaud, PhD2,3, Claudio Perret, PhD1, Tanja H. Kakebeeke, PhD1, Kenneth J. Hunt PhD2,3 and Prisca Eser, PhD4From the 1Swiss Paraplegic Research, Nottwil, Switzerland, 2University of Glasgow, Glasgow, UK, 3Queen Elizabeth National Spinal Injuries Unit, Glasgow, UK and the 4Department of Rheumatology and Clinical  Immunology/Allergology, University Hospital Bern, Berne, Switzerland2 A. Frotzler et al.SubjectsEleven people with a chronic SCI participated in a high-volume FES-cycling programme (up to 5 sessions per week, for one year) as published previously (6). Of those, 4 men and one woman aged 38.6 (standard deviation (SD) 8.1) years (age range 27.7–48.4 years) who showed a significant training effect on bone parameters attended follow-up investigations after termination of the high-volume FES-cycling programme. All subjects had motor-complete post-traumatic paraplegia (grade AIS A, i.e. American Spinal Injury Association (ASIA) impairment scale (AIS) (7)), with a lesion level between T4 and T7 and a lesion duration of 11.4 (SD 7.0) years (range 3.6–19.8 years). Exclusion criteria were current or past unhealed bone fractures, diseases known to affect bone metabolism and use of bone acting drugs. All subjects were informed about the protocol for the bone measuring procedure and were required to sign an informed consent form. Reduced FES-cycle training or detraining At the end of the 12-month high-volume FES-cycling programme (for more training details see Frotzler et al. (6)), subjects were free to stop or continue the FES-cycling at their own desired training volume (as determined by the number and duration of sessions per week and the training intensity, i.e. resistance). Four subjects stopped the FES-cycling programme and one subject decided to continue a reduced FES-cycle training and performed 2–3 training sessions per week, each lasting 30 min.MeasurementsBone and soft tissue measurements were performed with a pQCT scan-ner (model XCT 3000, Stratec Medical, Pforzheim, Germany) with regard to volumetric BMD and bone geometry, as well as muscle and fat cross-sectional areas. Image processing and calculation of numeri-cal values were performed using the manufacturer’s software package (version 6.0 B). Peripheral QCT scans were performed 4 times: at baseline prior to the FES-intervention (t1), at the end of the high- volume FES-cycling programme (t2), as well as after 6 (t3) and 12 months (t4) of detraining or reduced training. Bone data at t1 and t2 have been published previously (6). In the tibial and femoral epiphyses, BMC, total BMD (BMDtot) and trabecular BMD (BMDtrab) were calculated. In the diaphyses, BMC and cortical BMD (BMDcort) were calculated. In addition, muscle cross-sectional area (CSAmuscle) and fat CSA (CSAfat) both in the thigh and the shank were also identified. Statistical analysisDue to the small number of subjects, only descriptive statistics were performed. The mean and SD of the changes in bone and soft tissue parameters between t2 and t3, and between t3 and t4 were calculated to analyse the impact of detraining or reduced FES-cycling. To describe the effect of detraining or reduced FES-cycling, changes in bone and soft tissue parameters between t1 and t2 were compared with those between t2 and t4.RESULTSImpact of detraining on bone and soft tissue Within 12 months of detraining, a mean of 73.0% (SD 13.4) of the total bone gain achieved between t1 and t2 in BMDtrab in the distal femur was still preserved at t4 (Fig. 1). At this site, 63.8% (SD 8.0) gained in BMDtot and 59.4% (SD 3.9) gained in BMC during the FES-cycling period were also preserved at t4. In the femoral shaft, BMC and BMDcort decreased by 1.8% (SD 0.8) and 3.6% (SD 2.8) between t2 and t4, which is comparable to the decreases in this site found between t1 and t2. With regard to the impact of detraining on soft tissue in the thigh, 22.1% (SD 21.0) of the total increase in CSAmuscle achieved between t1 and t2 was preserved after 12 months of detraining. The main decrease of the total gain in CSAmuscle (68.6% (SD 34.0)) occurred within the first 6 months of detraining, i.e. between t2 and t3. CSAfat in the thigh did not change considerably during the FES-cycling programme, but increased in the phase of de-training and was, on average, 7.6% higher at t4 than at t1. With regard to the impact of detraining on the tibia, bone parameters at this site only changed by between –1.3% and 1.6%. This is similar to the negligible bone changes found during the high-volume FES-cycling programme between t1 and t2. Soft tissue parameters in the lower leg also showed only minor changes between t2 and t4: both CSAmuscle and CSAfat increased on average by 3.2% and 3.5%. Impact of reduced FES-cycling on bone and soft tissue One subject continued a reduced FES-cycle training programme between t2 and t4 and was able to preserve 96.2% and 95.0% of the total gain in distal femoral BMDtot and distal femoral BMDtrab (Fig. 1) achieved during high-volume FES-cycling. In the femoral shaft, BMC and BMDcort decreased by 7.3% and 5.4%, respectively, between t2 and t4. It should be noted that BMC at this site showed similar decreases during high-volume FES-cycling, i.e. between t1 and t2. With regard to the impact of reduced FES-cycling on the soft tissue in the thigh, both CSAmuscle and CSAfat decreased by 1.5% and 17.0%. Thus, nearly the complete gain in muscle tissue achieved during high-volume FES-cycling was still preserved at t4. In the tibial epiphysis and diaphysis, bone parameters showed decreases of between 1.3% and 4.8% in the phase of reduced FES-cycling. Interestingly, these decreases are less pronounced than those observed in this subject during high-volume FES-cycling with decreases in tibial bone parameters of up to 18.6%. Fig. 1. Adaptive changes in trabecular bone mineral density (BMD) of the distal femur. Values are shown at baseline (t1), after 12 months of high-volume functional electrical stimulation (FES)-cycling (t2), and after 6 (t3) and 12 months (t4) of detraining or reduced FES-cycle training. Note that one subject (black line) continued reduced FES-cycling between t2 and t4, whilst 4 participants (grey lines) stopped high-volume FES-cycling at t2. The dashed line indicates the start of the detraining or reduced FES-cycling following high-volume FES-cycling.J Rehabil Med 413Bone and muscle parameters after FES-cycling in SCI DISCUSSIONThe effect of detraining or reduced FES-cycle training fol-lowing 12 months of high-volume FES-cycling on bones in the lower extremities of 5 persons with chronic complete SCI was investigated. This is the first study with such a long FES-intervention and follow-up period and the first to measure bone and soft-tissue parameters by pQCT. Despite the small number of subjects the present study shows a clear tendency: between 59% and 73% of the gain achieved in BMC, BMDtot and BM-Dtrab in the distal femoral epiphysis following high-volume FES-cycling were still preserved after 12 months of detraining. This finding is in contrast to the documentations of Chen et al. (5), who found that after stopping FES-cycling (from 5 to zero FES-cycle training sessions per week) bone values returned to baseline levels within 6 months of detraining. According to our results, it appears to take more than 12 months of detraining to resorb the bone tissue that was gained within 12 months of high-volume FES-cycling. In addition, according to Wilmet et al. (8) who found a decrease of BMC of approximately 4% per month in areas rich in trabecular bone during the first year of SCI, bone loss following high-volume FES-cycling in people with chronic SCI seems to be slower with an average decrease in distal femoral BMC of 0.5% per month. The reason for this finding remains unclear, and needs to be investigated in further studies. We speculate that factors that affect bone metabolism, such as vascular atrophy after SCI, may slow down bone loss in people with chronic SCI. Regarding the muscle tissue in the paralysed legs, more than two-thirds of the muscle gain achieved during high-volume FES-cycling was lost within one year of detraining. This is comparable to the atrophy in CSAmuscle found in people after acute SCI (9). Reduced FES-cycle training (2.5 training sessions of 30 min per week) seemed to preserve the increase in both the bone at the distal femur and the muscle tissue of the thigh that resulted from high-volume FES-cycling. The present results are in contrast to the findings of Mohr et al. (4), who found the total gain in areal BMD (+10%) in the proximal tibia following FES-cycling for 30 min per day, 3 days per week for 12 months to be lost after a further 6 months with only one training session per week. It may be that there is an important difference between 1 and 2 training sessions per week, with one weekly training session turning a bone’s disuse mode “on”, thus resulting in resorption of the gained bone substance (as described by Frost (10)). According to Frost’s Mechanostat-theory (10), load-induced strains in bones provide the primary control signal underlying the biological responses of bone to its mechanical usage. Thus, strains above a certain threshold turn modelling “on”, resulting in an increased bone mass and strength. On the other hand, if strains are too small or absent, a disuse mode of remodelling turns “on” and bone will be resorbed until bone strength is adapted to its new mechanical usage. Consequently, one weekly training session may not be enough to preserve an adequate muscle mass necessary to induce large enough bone strains, while 2 sessions per week may preserve the previously achieved gain in muscle mass sufficiently in order to preserve the achieved gain in BMC. Several studies documented the fact that people with SCI are at a higher risk of low-trauma fractures (3), and that fractures mainly occur in the distal femur and in the distal and proximal tibia (11). Since fractures may lead to comorbidity and a reduc-tion in quality of life, improvement of bone parameters in the femur may have considerable clinical relevance. High-volume FES-cycling has the potential to increase bone strength of the distal femur in people with chronic and complete SCI (6). Hence, we assume that fracture risk at this site might be reduced after high-volume FES-cycle training and that this protective effect is subsequently sustained following a period of reduced FES-cycling, or even after 12 months of detraining. Indeed, the BMDtrab in the distal femur is reported to be the most sensi-tive bone parameter distinguishing between SCI persons with and without fractures (11). Four of our subjects had baseline BMDtrab values in the distal femur below the reported fracture threshold (11). However, at the end of the 30-month period of monitoring (including 12 months of high-volume FES-cycling and 12 months of detraining or reduced FES-cycling), all of our subjects, independent of whether they stopped or continued FES-cycling, remained above this fracture threshold. Thus, for a lasting improvement in bone parameters in the distal femur of people with chronic complete SCI we recommend a 2-phase FES-cycle training schedule, the first phase consisting of high-volume FES-cycle training in order to increase bone parameters, followed by the second phase consisting of reduced FES-cycle training in order to preserve bone parameters. Studies with even longer follow-up periods are needed to determine how long this second phase of reduced training volume may be.ACKNOWLEDGEMENTSWe gratefully acknowledge all subjects who participated in the study for dedicating their time and effort. This work was supported by the Engi-neering and Physical Sciences Research Council (grants GR/R92462, Glasgow) and the Swiss Paraplegic Foundation. REFERENCES1. Biering-Sorensen F, Bohr HH, Schaadt OP. Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury. Eur J Clin Invest 1990; 20: 330–335.2. Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, et al. Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 2004; 34: 869–880.3. Vestergaard P, Krogh K, Rejnmark L, Mosekilde L. Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord 1998; 36: 790–796.4. Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M. Increased bone mineral density after prolonged elec-trically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int 1997; 61: 22–25.5. Chen SC, Lai CH, Chan WP, Huang MH, Tsai HW, Chen JJ. Increases in bone mineral density after functional electrical stimu-lation cycling exercises in spinal cord injured patients. Disabil Rehabil 2005; 27: 1337–1341.6. Frotzler A, Coupaud S, Perret C, Kakebeeke TH, Hunt KJ, Donaldson N de N, et al. High-volume FES-cycling partially re-J Rehabil Med 414 A. Frotzler et al.verses bone loss in people with chronic spinal cord injury. Bone 2008; 43: 169–176.7. Maynard FM Jr., Bracken MB, Creasey G, Ditunno JF Jr., Donovan WH, Ducker TB, et al. International Standards for Neurological and Functional Classification of Spinal Cord Injury. American Spinal Injury Association. Spinal Cord 1997; 35: 266–274.8. Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P. Longitudinal study of the bone mineral content and of soft tis-sue composition after spinal cord section. Paraplegia 1995; 33: 674–677.9. Castro MJ, Apple DF Jr., Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol 1999; 80: 373–378.10. Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec 1987; 219: 1–9.11. Eser P, Frotzler A, Zehnder Y, Denoth J. Fracture threshold in the femur and tibia of people with spinal cord injury as determined by peripheral quantitative computed tomography. Arch Phys Med Rehabil 2005; 86: 498–504.J Rehabil Med 41

High-volume FES-cycling partially reJ Rehabil Med 414 A. Frotzler et al. verses bone loss in people with chronic spinal cord injury.

Effect of detraining on bone and muscle tissue in subjects with chronic spinal cord injury after a period of electrically-stimulated cycling: a small cohort study

Enlighten: Publications

 
 
 
 
 
 
Frotzler, A. and Coupaud, S. and Perret, C. and Kakebeeke, T.H. and 
Hunt, K.J. and Eser, P. (2009) Effect of detraining on bone and muscle 
tissue in subjects with chronic spinal cord injury after a period of 
electrically-stimulated cycling: a small cohort study. Journal of 
Rehabilitation Medicine, 41(4). pp. 282-285. ISSN 1650-1977 
 
 
http://eprints.gla.ac.uk/4938/ 
 
Deposited on: 24 March 2009 
 
 
Enlighten – Research publications by members of the University of Glasgow 
http://eprints.gla.ac.uk 
ORIGINAL REPORT
J Rehabil Med 2009 Preview
J Rehabil Med 41© 2009 The Authors. doi: 10.2340/16501977-0321
Journal Compilation © 2009 Foundation of Rehabilitation Information. ISSN 1650-1977
Objective: To investigate adaptive changes in bone and 
muscle parameters in the paralysed limbs after detraining 
or reduced functional electrical stimulation (FES) induced 
cycling following high-volume FES-cycling in chronic spinal 
cord injury. 
Subjects: Five subjects with motor-sensory complete spinal 
cord injury (age 38.6 years, lesion duration 11.4 years) were 
included. Four subjects stopped FES-cycling completely 
after the training phase whereas one continued reduced 
FES-cycling (2–3 times/week, for 30 min).
Methods: Bone and muscle parameters were assessed in the 
legs using peripheral quantitative computed tomography at 6 
and 12 months after cessation of high-volume FES-cycling. 
Results: Gains achieved in the distal femur by high-volume 
FES-cycling were partly maintained at one year of detrain-
ing: 73.0% in trabecular bone mineral density, 63.8% in to-
tal bone mineral density, 59.4% in bone mineral content and 
22.1% in muscle cross-sectional area in the thigh. The sub-
ject who continued reduced FES-cycling maintained 96.2% 
and 95.0% of the previous gain in total and trabecular bone 
mineral density, and 98.5% in muscle cross-sectional area. 
Conclusion: Bone and muscle benefits achieved by one year 
of high-volume FES-cycling are partly preserved after 12 
months of detraining, whereas reduced cycling maintains 
bone and muscle mass gained. This suggests that high-
 volume FES-cycling has clinical relevance for at least one 
year after detraining. 
Key words: bone loss, detraining, functional electrical stimula-
tion, osteoporosis, spinal cord injury.
J Rehabil Med 2008; 00: 00–00
Correspondence address: Sylvie Coupaud, Centre for Reha-
bilitation Engineering, Department of Mechanical Engineer-
ing, University of Glasgow, Glasgow G12 8QQ, UK. E-mail: 
s.coupaud@mech.gla.ac.uk 
Submitted July 14, 2008; accepted October 10, 2008
INTRODUCTION
Spinal cord injury (SCI) leads to a rapid and distinct reduction 
in bone tissue in the paralysed regions (1). The most affected 
areas are the metaphyseal-epiphyseal regions of the distal 
femur, and of both the proximal and distal tibia, where bone 
mineral content (BMC) is reduced by approximately 50% 
and 70%, respectively, within the first few years post-injury 
(2). The clinical significance of this bone loss and associated 
reduction in bone strength is that it exposes those with SCI 
to a high risk of low-energy fractures, with a lifetime risk of 
suffering a fracture in the lower limbs being twice as high as 
in able-bodied people (3). 
In order to increase bone strength in the paralysed limbs 
and reduce fracture risk, the application of load on bones in 
people with SCI was investigated. Active loading i.e. through 
muscle contractions by means of functional electrical stimula-
tion (FES)-induced cycling was found to lead to a site-specific 
recovery in bone mineral density (BMD) in the paralysed 
legs up to 14% (4–6). However, despite the positive effect of 
FES-cycling on bones after SCI, little is known about bone 
behaviour in the paralysed limbs once the FES-cycling is 
discontinued. To our knowledge only 2 groups (4, 5) have as 
yet investigated the impact of a reduced FES-cycle training 
programme or detraining on bone status in the paralysed limbs. 
Both groups found that the partially reversed bone loss after 
initial FES-cycling was lost within the subsequent 6 months of 
either reduced FES-cycling or detraining. However, whether 
an initial phase of high-volume FES-cycling causes similar 
bone adaptations during detraining or reduced FES-cycling 
remains unclear.
The aim of the present study was therefore to investigate the 
impact of detraining or reduced FES-cycling following a one-
year high-volume FES-cycle training on bones and soft tissue 
in the paralysed limbs of people with chronic complete SCI by 
detailed peripheral quantitative computed tomography (pQCT) 
assessment. For this purpose, we performed a follow-up study of 
the subjects who participated in the previously published study 
on the osteogenic effects of high-volume FES-cycling (6). 
MATERIALS AND METHODS
The study was conducted as a multi-centre design at the Queen Elizabeth 
National Spinal Injuries Unit and the University of Glasgow, Glasgow, 
UK as well as at the Swiss Paraplegic Research, Nottwil, Switzerland. 
The study was approved by the local ethics committees. 
EFFECT OF DETRAINING ON BONE AND MUSCLE TISSUE IN 
SUBJECTS WITH CHRONIC SPINAL CORD INJURY AFTER A PERIOD OF 
ELECTRICALLY-STIMULATED CYCLING: A SMALL COHORT STUDY
Angela Frotzler, PhD1, Sylvie Coupaud, PhD2,3, Claudio Perret, PhD1, Tanja H. Kakebeeke, 
PhD1, Kenneth J. Hunt PhD2,3 and Prisca Eser, PhD4
From the 1Swiss Paraplegic Research, Nottwil, Switzerland, 2University of Glasgow, Glasgow, UK, 3Queen Elizabeth 
National Spinal Injuries Unit, Glasgow, UK and the 4Department of Rheumatology and Clinical  
Immunology/Allergology, University Hospital Bern, Berne, Switzerland
2 A. Frotzler et al.
Subjects
Eleven people with a chronic SCI participated in a high-volume 
FES-cycling programme (up to 5 sessions per week, for one year) 
as published previously (6). Of those, 4 men and one woman aged 
38.6 (standard deviation (SD) 8.1) years (age range 27.7–48.4 years) 
who showed a significant training effect on bone parameters attended 
follow-up investigations after termination of the high-volume FES-
cycling programme. All subjects had motor-complete post-traumatic 
paraplegia (grade AIS A, i.e. American Spinal Injury Association 
(ASIA) impairment scale (AIS) (7)), with a lesion level between T4 
and T7 and a lesion duration of 11.4 (SD 7.0) years (range 3.6–19.8 
years). Exclusion criteria were current or past unhealed bone fractures, 
diseases known to affect bone metabolism and use of bone acting drugs. 
All subjects were informed about the protocol for the bone measuring 
procedure and were required to sign an informed consent form. 
Reduced FES-cycle training or detraining 
At the end of the 12-month high-volume FES-cycling programme 
(for more training details see Frotzler et al. (6)), subjects were free to 
stop or continue the FES-cycling at their own desired training volume 
(as determined by the number and duration of sessions per week and 
the training intensity, i.e. resistance). Four subjects stopped the FES-
cycling programme and one subject decided to continue a reduced 
FES-cycle training and performed 2–3 training sessions per week, 
each lasting 30 min.
Measurements
Bone and soft tissue measurements were performed with a pQCT scan-
ner (model XCT 3000, Stratec Medical, Pforzheim, Germany) with 
regard to volumetric BMD and bone geometry, as well as muscle and 
fat cross-sectional areas. Image processing and calculation of numeri-
cal values were performed using the manufacturer’s software package 
(version 6.0 B). Peripheral QCT scans were performed 4 times: at 
baseline prior to the FES-intervention (t1), at the end of the high- volume 
FES-cycling programme (t2), as well as after 6 (t3) and 12 months (t4) 
of detraining or reduced training. Bone data at t1 and t2 have been 
published previously (6). In the tibial and femoral epiphyses, BMC, 
total BMD (BMDtot) and trabecular BMD (BMDtrab) were calculated. 
In the diaphyses, BMC and cortical BMD (BMDcort) were calculated. 
In addition, muscle cross-sectional area (CSAmuscle) and fat CSA 
(CSAfat) both in the thigh and the shank were also identified. 
Statistical analysis
Due to the small number of subjects, only descriptive statistics were 
performed. The mean and SD of the changes in bone and soft tissue 
parameters between t2 and t3, and between t3 and t4 were calculated to 
analyse the impact of detraining or reduced FES-cycling. To describe 
the effect of detraining or reduced FES-cycling, changes in bone and 
soft tissue parameters between t1 and t2 were compared with those 
between t2 and t4.
RESULTS
Impact of detraining on bone and soft tissue 
Within 12 months of detraining, a mean of 73.0% (SD 13.4) of 
the total bone gain achieved between t1 and t2 in BMDtrab in the 
distal femur was still preserved at t4 (Fig. 1). At this site, 63.8% 
(SD 8.0) gained in BMDtot and 59.4% (SD 3.9) gained in BMC 
during the FES-cycling period were also preserved at t4. In the 
femoral shaft, BMC and BMDcort decreased by 1.8% (SD 0.8) 
and 3.6% (SD 2.8) between t2 and t4, which is comparable to 
the decreases in this site found between t1 and t2. With regard to 
the impact of detraining on soft tissue in the thigh, 22.1% (SD 
21.0) of the total increase in CSAmuscle achieved between t1 
and t2 was preserved after 12 months of detraining. The main 
decrease of the total gain in CSAmuscle (68.6% (SD 34.0)) 
occurred within the first 6 months of detraining, i.e. between t2 
and t3. CSAfat in the thigh did not change considerably during 
the FES-cycling programme, but increased in the phase of de-
training and was, on average, 7.6% higher at t4 than at t1. With 
regard to the impact of detraining on the tibia, bone parameters 
at this site only changed by between –1.3% and 1.6%. This is 
similar to the negligible bone changes found during the high-
volume FES-cycling programme between t1 and t2. Soft tissue 
parameters in the lower leg also showed only minor changes 
between t2 and t4: both CSAmuscle and CSAfat increased on 
average by 3.2% and 3.5%. 
Impact of reduced FES-cycling on bone and soft tissue 
One subject continued a reduced FES-cycle training programme 
between t2 and t4 and was able to preserve 96.2% and 95.0% 
of the total gain in distal femoral BMDtot and distal femoral 
BMDtrab (Fig. 1) achieved during high-volume FES-cycling. 
In the femoral shaft, BMC and BMDcort decreased by 7.3% 
and 5.4%, respectively, between t2 and t4. It should be noted 
that BMC at this site showed similar decreases during high-
volume FES-cycling, i.e. between t1 and t2. With regard to the 
impact of reduced FES-cycling on the soft tissue in the thigh, 
both CSAmuscle and CSAfat decreased by 1.5% and 17.0%. 
Thus, nearly the complete gain in muscle tissue achieved during 
high-volume FES-cycling was still preserved at t4. In the tibial 
epiphysis and diaphysis, bone parameters showed decreases of 
between 1.3% and 4.8% in the phase of reduced FES-cycling. 
Interestingly, these decreases are less pronounced than those 
observed in this subject during high-volume FES-cycling with 
decreases in tibial bone parameters of up to 18.6%. 
Fig. 1. Adaptive changes in trabecular bone mineral density (BMD) of the 
distal femur. Values are shown at baseline (t1), after 12 months of high-
volume functional electrical stimulation (FES)-cycling (t2), and after 6 (t3) 
and 12 months (t4) of detraining or reduced FES-cycle training. Note that 
one subject (black line) continued reduced FES-cycling between t2 and 
t4, whilst 4 participants (grey lines) stopped high-volume FES-cycling at 
t2. The dashed line indicates the start of the detraining or reduced FES-
cycling following high-volume FES-cycling.
J Rehabil Med 41
3Bone and muscle parameters after FES-cycling in SCI 
DISCUSSION
The effect of detraining or reduced FES-cycle training fol-
lowing 12 months of high-volume FES-cycling on bones in 
the lower extremities of 5 persons with chronic complete SCI 
was investigated. This is the first study with such a long FES-
intervention and follow-up period and the first to measure bone 
and soft-tissue parameters by pQCT. Despite the small number 
of subjects the present study shows a clear tendency: between 
59% and 73% of the gain achieved in BMC, BMDtot and BM-
Dtrab in the distal femoral epiphysis following high-volume 
FES-cycling were still preserved after 12 months of detraining. 
This finding is in contrast to the documentations of Chen et al. 
(5), who found that after stopping FES-cycling (from 5 to zero 
FES-cycle training sessions per week) bone values returned to 
baseline levels within 6 months of detraining. According to our 
results, it appears to take more than 12 months of detraining 
to resorb the bone tissue that was gained within 12 months of 
high-volume FES-cycling. In addition, according to Wilmet et 
al. (8) who found a decrease of BMC of approximately 4% per 
month in areas rich in trabecular bone during the first year of 
SCI, bone loss following high-volume FES-cycling in people 
with chronic SCI seems to be slower with an average decrease 
in distal femoral BMC of 0.5% per month. The reason for this 
finding remains unclear, and needs to be investigated in further 
studies. We speculate that factors that affect bone metabolism, 
such as vascular atrophy after SCI, may slow down bone loss 
in people with chronic SCI. Regarding the muscle tissue in 
the paralysed legs, more than two-thirds of the muscle gain 
achieved during high-volume FES-cycling was lost within 
one year of detraining. This is comparable to the atrophy in 
CSAmuscle found in people after acute SCI (9). Reduced 
FES-cycle training (2.5 training sessions of 30 min per week) 
seemed to preserve the increase in both the bone at the distal 
femur and the muscle tissue of the thigh that resulted from 
high-volume FES-cycling. The present results are in contrast 
to the findings of Mohr et al. (4), who found the total gain in 
areal BMD (+10%) in the proximal tibia following FES-cycling 
for 30 min per day, 3 days per week for 12 months to be lost 
after a further 6 months with only one training session per 
week. It may be that there is an important difference between 
1 and 2 training sessions per week, with one weekly training 
session turning a bone’s disuse mode “on”, thus resulting in 
resorption of the gained bone substance (as described by Frost 
(10)). According to Frost’s Mechanostat-theory (10), load-
induced strains in bones provide the primary control signal 
underlying the biological responses of bone to its mechanical 
usage. Thus, strains above a certain threshold turn modelling 
“on”, resulting in an increased bone mass and strength. On the 
other hand, if strains are too small or absent, a disuse mode of 
remodelling turns “on” and bone will be resorbed until bone 
strength is adapted to its new mechanical usage. Consequently, 
one weekly training session may not be enough to preserve an 
adequate muscle mass necessary to induce large enough bone 
strains, while 2 sessions per week may preserve the previously 
achieved gain in muscle mass sufficiently in order to preserve 
the achieved gain in BMC. 
Several studies documented the fact that people with SCI are 
at a higher risk of low-trauma fractures (3), and that fractures 
mainly occur in the distal femur and in the distal and proximal 
tibia (11). Since fractures may lead to comorbidity and a reduc-
tion in quality of life, improvement of bone parameters in the 
femur may have considerable clinical relevance. High-volume 
FES-cycling has the potential to increase bone strength of the 
distal femur in people with chronic and complete SCI (6). 
Hence, we assume that fracture risk at this site might be reduced 
after high-volume FES-cycle training and that this protective 
effect is subsequently sustained following a period of reduced 
FES-cycling, or even after 12 months of detraining. Indeed, the 
BMDtrab in the distal femur is reported to be the most sensi-
tive bone parameter distinguishing between SCI persons with 
and without fractures (11). Four of our subjects had baseline 
BMDtrab values in the distal femur below the reported fracture 
threshold (11). However, at the end of the 30-month period of 
monitoring (including 12 months of high-volume FES-cycling 
and 12 months of detraining or reduced FES-cycling), all of 
our subjects, independent of whether they stopped or continued 
FES-cycling, remained above this fracture threshold. Thus, for 
a lasting improvement in bone parameters in the distal femur 
of people with chronic complete SCI we recommend a 2-phase 
FES-cycle training schedule, the first phase consisting of high-
volume FES-cycle training in order to increase bone parameters, 
followed by the second phase consisting of reduced FES-cycle 
training in order to preserve bone parameters. Studies with even 
longer follow-up periods are needed to determine how long this 
second phase of reduced training volume may be.
ACKNOWLEDGEMENTS
We gratefully acknowledge all subjects who participated in the study for 
dedicating their time and effort. This work was supported by the Engi-
neering and Physical Sciences Research Council (grants GR/R92462, 
Glasgow) and the Swiss Paraplegic Foundation. 
REFERENCES
1. Biering-Sorensen F, Bohr HH, Schaadt OP. Longitudinal study 
of bone mineral content in the lumbar spine, the forearm and the 
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OBJECTIVE: To investigate adaptive changes in bone and muscle parameters in the paralysed limbs after detraining or reduced functional electrical stimulation (FES) induced cycling following high-volume FES-cycling in chronic spinal cord injury. SUBJECTS: Five subjects with motor-sensory complete spinal cord injury (age 38.6 years, lesion duration 11.4 years) were included. Four subjects stopped FES-cycling completely after the training phase whereas one continued reduced FES-cycling (2-3 times/week, for 30 min). METHODS: Bone and muscle parameters were assessed in the legs using peripheral quantitative computed tomography at 6 and 12 months after cessation of high-volume FES-cycling. RESULTS: Gains achieved in the distal femur by high-volume FES-cycling were partly maintained at one year of detraining: 73.0% in trabecular bone mineral density, 63.8% in total bone mineral density, 59.4% in bone mineral content and 22.1% in muscle cross-sectional area in the thigh. The subject who continued reduced FES-cycling maintained 96.2% and 95.0% of the previous gain in total and trabecular bone mineral density, and 98.5% in muscle cross-sectional area. CONCLUSION: Bone and muscle benefits achieved by one year of high-volume FES-cycling are partly preserved after 12 months of detraining, whereas reduced cycling maintains bone and muscle mass gained. This suggests that high-volume FES-cycling has clinical relevance for at least one year after detraining

Kakebeeke, Tanja H

Hunt, Kenneth J

Bern Open Repository and Information System (BORIS)

A Frotzler

S Coupaud

C Perret

TH Kakebeeke

KJ Hunt

P Eser

Crossref

Effect of detraining on bone and muscle tissue in subjects with chronic spinal cord injury after a period of electrically-stimulated cycling: A small cohort study

Name not available

Effect of detraining on bone and muscle tissue in subjects with chronic spinal cord injury after a period of electrically-stimulated cycling: a small cohort study

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