The effects of spinal cord injury and exercise on bone mass: A literature review

NeuroRehabilitation

Volumn 29, Issue 3, 2011, Pages 261-269

  Dolbow, D R ^a,b   Gorgey, A S ^a,b   Daniels, J A ^a   Adler, R A ^a,b   Moore, J R ^a   Gater Jr , D R ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cortical bone; functional electrical stimulation; Osteogenic osteoporosis; trabecular bone

Indexed keywords

AGING; BONE DEMINERALIZATION; BONE DENSITY; BONE MASS; EXERCISE; HUMAN; OSTEOLYSIS; OSTEOPOROSIS; PATHOPHYSIOLOGY; REVIEW; SPINAL CORD INJURY;

BONE AND BONES; BONE DENSITY; ELECTRIC STIMULATION THERAPY; EXERCISE THERAPY; HUMANS; OSTEOPOROSIS; PARALYSIS; SPINAL CORD INJURIES;

EID: 84863398789     PISSN: 10538135     EISSN: 18786448     Source Type: Journal    
DOI: 10.3233/NRE-2011-0702     Document Type: Review

References (75)

1. R.R. Menter, Aging with spinal cord injury. Spinal Cord Injury 1998; 9(1) http://www.thecni.org/reviews/09-1-p16-menter. htm. Retrieved 6/25/10.
2. M.G. Lazo, P. Shirazi, A. Giobbie-Hurder et al., Osteoporosis and risk of fracture in men with spinal cord injury, Spinal Cord 1(39) (2001), 208-214. (Pubitemid 32574770)
3. W. Sniger and E. Garshick, Alendronate increases bone density in chronic spinal cord injury: A case report, Arch Phys Med Rehabil 83(1) (2002), 139-140. (Pubitemid 34052152)
4. G. Demiril, H. Yilmaz, N. Parker et al., Osteoporosis after spinal cord injury, Spinal Cord 36 (1998), 822-825. (Pubitemid 29008175)
5. R. Biering-Sorensen and H. Bohr, Bone mineral content of the lumbar spine and lower extremities years after spinal cord lesion, Paraplegia 26 (1998), 293-301.
6. D.E. Garland, C.A. Stewart, R.H. Adkins et al., Osteoporosis after spinal cord injury, Journal of Orthop Res 10 (1992), 371-378.
7. S. Dudley-Javoroski and R.K. Shields, Muscle and Bone Plasticity After Spinal Cord Injury: Review of adaptation to disuse and to electrical muscle stimulation, Journal of Rehabil Res and Dev 45(2) (2008), 283-296.
8. B. Broholm, J. Podenphant and F. Biering-Sorensen, The course of bone mineral density and biochemical markers of bone turnover in early postmenopausal spinal cord-lesioned females, Spinal Cord 43 (2005), 674-677. (Pubitemid 41718910)
9. R.K. Shields, Muscular Skeletal and Neural adaptations Following Spinal Cord Injury, J of Orthopedaedic and Sports Physical Therapy 32(2) (2002), 65-74. (Pubitemid 34113515)
10. E. Wilmet, A. Ismail, A. Heilporn et al., Longitudinal study of bone mineral content and of soft tissue composition after spinal cord section, Paraplegia 33(11) (1995), 674-677.
11. M.S. Nash, Spinal Cord Injury, in: Exercise in Rehabilitation Medicine, (2nd ed.), W.R. Frontera, D.M. Slovik and D.M. Dawson, eds, Human Kinetics Inc. 2003, pp. 191-205.
12. P. Eser, A. Frotzler, Y. Zehnder et al., Relationships between the duration of paralysis and bone structure: A pQCT study of spinal cord injured individuals, Bone 34(5) (2004), 869-880. (Pubitemid 38581133)
13. M. Dauty, M. Perrouin and B. Verbe, Supralesional and sub-lesional bone mineral density in spinal cord injured patients, Bone 27(2) (2000), 305-309. (Pubitemid 30458827)
14. F.B. Sorensen, H. Bohr and O. Schaadt, Bone mineral content of the lumbar spine and lower extremities years after spinal cord lesion, Paraplegia 26 (1998), 293-301.
15. R.K. Shields, S. Dudley-Javorski and K.M. Boaldin, Peripheral quantitative computed tomography: Measurement sensitivity in persons with and without spinal cord injury, Arch Phys Med Rehabil 87(10) (2006), 1376-1381. (Pubitemid 44470765)
16. D.R. Gater, Jr., Spinal Cord Injury, in: Clincal Exercise Physiology, (1st ed.), J.K. Ehrman, P.M. Gordon, P.S. Visich and S.J. Keteyian, eds, Human Kinetics Inc. Champaign, IL, 2003, pp. 503-526.
17. J. Rittweger, K. Jerris, T. Altenburg et al., Bone adaptation to altered loading after spinal cord injury: A study of bone and muscle strength, Journal of Musculoskeletal Neuronal Interact 6(3) (2006), 269-276. (Pubitemid 44650786)
18. W.A. Bauman, A.M. Spungen, J. Wang et al., Continuous loss of bone during chronic immobilization: a monozygotic twin study, Osteoporosis Int 10(2) (1999), 123-127. (Pubitemid 29462200)
19. D.E. Garland, R.H. Adkins and C.A. Stewart, Regional osteoporosis in women who have a complete spinal cord injury, Journal of Bone and Joint Surgery 83A(8) (2001), 1195-1200. (Pubitemid 32735070)
20. L. Giangregorio and N. McCartney, Bone loss and muscle atrophy in spinal cord injury: epidemiology, fracture prediction, rehabilitation strategies, J Spinal Cord Med 29(5) (2006), 489-500.
21. L.M. Jones, M. Legge and A. Goulding, Intensive exercise may preserve bone mass of the upper limbs in spinal cord injured males but does not retard demineralization of the lower body, Spinal Cord 40 (2002), 230-235. (Pubitemid 34499304)
22. K. Kutulus, A. Canan, O. Sumru et al., Evaluation of bone Mineral Density in Patients With Spinal Cord Injury, Journal of Spinal Cord Medicine 29(4) (2006), 396-401.
23. Y.-C. Wang, Y.-H. Wang, S. Ting-Fang et al., Sublesional spinal vertebral bone mineral density correlates with nuro-logical level of body mass index, in individuals with chronic complete spinal cord injuries, Spine 35(9) (2010), 958-962.
24. F. Biering-Sorensen, B. Hansen, B.S. Lee et al., Non-parmacological treatment and prevention of bone loss after spinal cord injury: a systematic review, Spinal Cord 47(7) (2009), 73-94.
25. S.L. Bonnick and L.A. Lewis, An overview of osteoporosis, in: Bone Densitometry for Technologists, Humana Press, N.J. Totowa, (2nd ed.), 2006, pp. 257-288.
26. J. Svircev, Osteoporosis and spinal cord injury. SCI Forum Report. Presented October 9, 2007. http://sci.washington.edu/info/forums/reports/ oestoporosis.asp Retrieved 6/11/2010.
27. H.M. Frost, The new bone: some anthropological potentials, Yearbook Phys Anthrop 28 (1985), 211-226. (Pubitemid 16171566)
28. T.N. Hangartner, M.M. Rodgers, R.M. Glaser et al., Tibial bone density loss in spinal cord injured patients: effects of FES exercise, Journal of Rehabil Res Dev 31 (1994), 50-61. (Pubitemid 24114617)
29. C.M. Modlesky, S. Majumdar, A. Narasimhan et al., Trabec-ular bone microarchitecture is deteriorated in men with spinal cord injury, Journal of Bone Mineral Research 19(1) (2004), 48-55. (Pubitemid 41295137)
30. P. Frey-Rindova, E.D. de Bruin, E. Stussi et al., Bone mineral density in upper and lower extremities during 12 months after spinal cord injury measured by peripheral quantitative computed tomography, Spinal Cord 38 (2000), 26-32. (Pubitemid 30142553)
31. S.M. Szollar, E.M. Martin, D.J. Sartoris et al., Bone Mineral Density and Indexes of Bone Metabolism in Spianl Cord Injury, Am Journal of Phys Med Rehabil 77 (1998), 28-35. (Pubitemid 28113367)
32. S.L. Bonnick and L.A. Lewis, An overview of osteoporosis, in: Bone Densitometry for Technologists, Humana Press, N.J. Totowa, (2nd ed.), 2006, pp. 257-288.
33. L.R. Morse, R.A. Battaglino, K.L. Stolzmann et al., Osteo-porotic fractures and hospitalization risk in chronic spinal cord injury, Osteoporos Int 20(3) (2009), 385-392.
34. D. Krueger, J. Caudill, J. Colquhoun et al., Bone Denistometry Course: Technologists course syllabus and associated reading materials. The International Society for Clinical Densitometry, 2010, pp. 9.
35. F.M. Maynard, R.S. Karunas, R.H. Adkins et al., Management of the Neuromuscular System, in: Spinal Cord Injury: Clinical Outcomes of the Model Systems, S.L. Stover, J.A. Delisa and G.G. Whiteneck, eds, Aspen, Gaitersburg, MD. 1995, pp. 163-169.
36. P. Eser, A. Frotzler, Y. Zehnder et al., Fracture threshold in the femur and tibia of people with spinal cord injury as determined by peripheral quantitative computed tomography, Arch Phys Med Rehabil 86(3) (2005), 498-504. (Pubitemid 40326632)
37. D.E. Garland and R.H. Adkins, Bone loss at the knee in spinal cord injury, Topics in Spinal Cord Injury Rehab 6 (2001), 37-46. (Pubitemid 32105175)
38. R. Levi, C. Hultling and A. Seiger, The Stockholm spinal cord injury study: 2. Associations between clinical patient characteristics and post-acute medical problems, Paraplegia 33(10), 585-594; in: Spinal Cord Injury: Functional Rehabilitation, (ed) M. Somers, F. Prentice Hall, Upper Saddle River, NJ 2nd Ed., 2001, p. 34.
39. B. Yilmaz, E. Yasar, A.S. Goktepe et al., The relationship between basal metabolic rate and femur bone mineral density in men with traumatic spinal cord injury, Arch Phys Med Rehabil 88(6) (2007), 758-761. (Pubitemid 46802397)
40. D. Rodrigues and H. Guilherme, Physiotherapy resources on bone mineral density loss prevention in patients with spinal cord injuries, Acta Ortopedica Brasileira 12(3) (2004).
41. R.K. Shields and S. Dudley-Javoroski, Musculoskeletal Plasticity after Acute Spinal Cord Injury: Effects of Long-Term Neuromuscular Electrical Stimulation Training J Neurophys-iol, 2006, http://jn.physiology.org/cgi/ reprint/01181.2005v1. pdf Retrieved on 6/12/2010.
42. D. Weiss, Osteoporosis and Spinal Cord Injury. 2008, http://emedicine. medscape.com/article/322204-overview Retrieved 6/9/2010.
43. B. Chen and A. Stein, Osteoporosis in Acute Spinal Cord Injury, Top Spinal Cord Inj Rehabil 9(1) (2003), 26-35. (Pubitemid 36667629)
44. B. Chen, J.I. Mechanicvk, D.M. Nierman et al., Combined calcitriol-pamidronate therapy for bone hyperresorption in spinal cord injury, Journal of Spinal Cord Med 24 (2001), 235-240. (Pubitemid 37484213)
45. J.I. Mechanick, F. Pomerantz, S. Flanagan et al., Parathyroid hormone suppression in spinal cord injury patients is associated with degree of neurologic impairment and not the level of injury, Arch Phys Med Rehabil 78 (1997), 692-696. (Pubitemid 27295112)
46. L. Maimoun, I. Couret, J.P. Micallef et al., Use of bone biochemical markers with dual-energy X-ray absorptiometry for early determination of bone loss in persons with spinal cord injury, Metabolism 51 (2002), 958-963.
47. J. Claus-Walker, R.E. Carter, R.J. Compos et al., Hypercal-cemia in early traumatic quadriplegia, J Chronic Dis 28(2) (Feb 1975), 81-90.
48. G.J. Merli, G.E. McElwain, A.G. Adler et al., Immobilization hypercalcemia in acute spinal cord injury treated with etidronate, Arch Intern Med 144(6) (1984), 1286-1288. (Pubitemid 14121083)
49. P. Frey-Rindova, E.D. De Bruin, E. Stussi et al., Bone mineral density in upper and lower extremities during 12 months after spinal cord injury measured by peripheral quantitative computed tomography, Spinal Cord 38(1) (2000), 26-32. (Pubitemid 30142553)
50. H. Kondo, A. Nifuji, S. Takeda et al., Unloading induces osteoblastic cell suppression and osteoclastic cell activation to lead to bone loss via sympathetic nervous system, J Biol Chem 280(34) (2005), 30192-30210.
51. R. Levasseur, J.P. Sabatier, C. Potrel-Burgot et al., Sympathetic nervous system as transmitter of mechanical loading in bone, Joint Bone Spine 70(6) (2003), 515-519. (Pubitemid 38029805)
52. C.M. Serre, D. Farley, P.D. Delmas et al., Evidence for a dense and intimate innervations of the bone tissue, including glutamate-containing fibers, Bone 25(6) (1999), 623-629.
53. M. Arai, T. Nagasawa, Y. Koshihara et al., Effects of beta-adrenergic agonists on bone-resorbing activity in human osteoclast-like cells, Biochem Biophys 1640(2-3) (2003), 137-142. (Pubitemid 36555699)
54. A. Chatraine, B. Nusgens and M. Lapiere, Bone remodeling during the development of osteoporosis in paraplegia. Calcif, Tissue Int 38 (1986), 323-327. (Pubitemid 16081449)
55. A. Chatraine, C. Van Ouwenaller et al., Intramedullary pressure and intraosseous phlebography in paraplegia, Paraplegia 17 (1979), 391-397.
56. H.M. Frost, "Mass" and the "mechanostat": a proposal, Anat Rec 219 (1987), 1-9.
57. H.M. Frost, Bone's mechanostat: a 2003 update, Anat Rec A Discov Mol Cell Evol Biol 275 (2003), 1081-1101. (Pubitemid 37486785)
58. J.J. Eng, S.M. Levins, A.F. Townson et al., Use of prolonged standing for individuals with spinal cord injury, Physical Therapy 81(8) (2001), 1392.
59. I. Lofvenmark, L. Werhagen and C. Norrbrink, Spasticity and bone density after a spinal cord injury, Journal of Rehabilitation Medicine 41(13) (2009), 1080-1084.
60. A.S. Goktepe, I. Tugcu, B. Yilmaz et al., Does standing Protect Bone Density in Patients With Chronic Spinal Cord Injury, Journal of Spinal Cord Medicine 31(2) (2008), 197-201. (Pubitemid 351951356)
61. C.F. Kunkel, A.M. Scremin, B. Eisenberg et al., Effect of "standing" on spasticity, contracture, and osteoporosis in paralyzed males, Arch Phys Med Rehabil 74 (1993), 73-78.
62. S. Goemaere, M. Van Laere, P. De Neve et al., Bone mineral status in paraplegic patients who do or do not perform standing, Osteoporosis Int 4 (1994), 138-143. (Pubitemid 24163545)
63. L.M. Giangregorio, A.L. Hicks, C.E. Webber et al., Body Weight supported treadmill training in acute spinal cord injury: impact on muscle and bone, Spinal Cord 43 (2005), 649-657. (Pubitemid 41718907)
64. E.M. Leeds, K.J. Klose, W. Ganz et al., Bone mineral density after bicycle ergometry training, Arch Phys Med Rehabil 71 (1990), 207-209. (Pubitemid 20093524)
65. B.M. Needham-Shropshire, J.G. Broton, K.J. Klose et al., Eva-lution of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 3. Lack of effect on bone mineral density, Arch Phys Med Rehabil 74 (1993), 73-78.
66. M.M. Rodgers, R.M. Glaser, S.F. Figoni et al., Musculoskele-tal responses of spinal cord injured individuals to functional neuromuscular stimulation-induced knee extension exercise training, Journal of Rehabil Res Dev 28 (1991), 19-26.
67. T. Mohr, J. Podenplant, F. Biering-Sorenen et al., Increased bone mineral density after prolonged electrically induced cy-cle training of paralyzed limbs in spinal cord injured man, Calcified Tissue International 61 (1997), 22-25. (Pubitemid 27262395)
68. S.A. Bloomfield, W.J. Mysiw and R.D. Jackson, Bone Mass and endocrine adaptations to training in spinal cord injury individuals, Bone 19 (1996), 61-68. (Pubitemid 26318747)
69. R.K. Shields, S. Dudley-Javoroski and L.A. Frey Law, Electrically induced muscle contractions influence bone density decline after spinal cord injury, Spine 31 (2006), 548-553.
70. R.K. Shields and S. Dudley-Javoroski, Musculoskeletal adaptations in chronic spinal cord injury: Effects of long term soleus electrical stimulation training, Neural Rehab Neural Repair 21 (2007), 169-179.
71. S.C. Chen, C.H. Lai, W.P. Chan et al., Increases in bone mineral density after functional electric stimulation cycling exercises in spinal cord injured patients, Disability and Rehabilitation 27(22) (2005), 1337-1341. (Pubitemid 41759382)
72. A. Frotzler, S. Coupland, C. Perret et al., High Volume FES cycling partially reverses bone loss in people with chronic spinal cord injury, Bone 43(1) (2008), 169-176.
73. X.-Y. Ruan, F.-Y. Jin, Y.-I., Liu et al., Effects of vibration therapy on bone mineral density in postmenopausal women with osteoporosis, Chinese Medical Journal 121(13) (2008), 1155-1158.
74. G. Melchiorri, A. Andreoli, E. Padua et al., Use of vibration exercise in spinal cord injury patients who regularly practice sport, Funct Neurol 22(3) (2007), 151-154. (Pubitemid 47611120)
75. K. Miyahara, D.H. Wang, K. Mori et al., Effect of sports activity on bone mineral density in wheelchair athletes, J Bone Miner Metab 26 (2008), 101-106. (Pubitemid 350308002)