Muscle and bone plasticity after spinal cord injury: Review of adaptations to disuse and to electrical muscle stimulation

Journal of Rehabilitation Research and Development

Volumn 45, Issue 2, 2008, Pages 283-296

  Dudley Javoroski, Shauna ^a   Shields, Richard K ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Adaptation; Bone; Electrical stimulation; Muscle; Musculoskeletal deterioration; Osteoporosis; Plasticity; pQCT; Rehabilitation; Soleus; Spinal cord injury

Indexed keywords

ADAPTATION; ELECTRICAL STIMULATION; MUSCULOSKELETAL DETERIORATION; OSTEOPOROSIS; PQCT; REHABILITATION; SOLEUS; SPINAL CORD INJURY;

BIOCHEMISTRY; BONE; DETERIORATION; DOSIMETRY; MINING; MUSCLE; PLASTICITY;

PATIENT REHABILITATION;

ADAPTATION; BONE; BONE DENSITY; HUMAN; MUSCLE; MUSCLE ATROPHY; MUSCLE EXCITATION; NEUROMUSCULAR ELECTRICAL STIMULATION; OSTEOPOROSIS; PLASTICITY; PRIORITY JOURNAL; REVIEW; SPINAL CORD INJURY; TRAINING; ANIMAL; BIOMECHANICS; ELECTROSTIMULATION THERAPY; INNERVATION; KINESIOTHERAPY; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOMECHANICS; BONE AND BONES; BONE DENSITY; ELECTRIC STIMULATION THERAPY; EXERCISE THERAPY; HUMANS; MUSCLE, SKELETAL; NEURONAL PLASTICITY; SPINAL CORD INJURIES;

EID: 56749115135     PISSN: 07487711     EISSN: 07487711     Source Type: Journal    
DOI: 10.1682/JRRD.2007.02.0031     Document Type: Review

References (149)

1. Stover SL, DeLisa JA, Whiteneck GG. Spinal cord injury: Clinical outcomes from the model systems. Gaithersburg (MD): Aspen Publishers, Inc; 1995.
2. Shields RK, Dudley-Javoroski S. Musculoskeletal deterioration and hemicorporectomy after spinal cord injury. Phys Ther. 2003;83(3):263-275
3. Wilmet E, Ismail AA, Heilporn A, Welraeds D, Bergmann P. Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia. 1995;33(11):674-677
4. Abramson AS. Bone disturbances in injuries to the spinal cord and cauda equina (paraplegia). J Bone Joint Surg. 1948;30:982-987
5. Claus-Walker J, Carter RE, Campos RJ, Spencer WA. Sitting, muscular exercises, and collagen metabolism in tetraplegia. Am J Phys Med. 1979;58(6):285-293
6. Issekutz B Jr, Blizzard JJ, Birkhead NC, Rodahl K. Effect of prolonged bed rest on urinary calcium output. J Appl Physiol. 1966;21(3):1013-1020
7. Kaplan PE, Roden W, Gilbert E, Richards L, Goldschmidt JW. Reduction of hypercalciuria in tetraplegia after weight-bearing and strengthening exercises. Paraplegia. 1981;19(5):289-293
8. Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve. 1984;7(9):691-699
9. Freeman LW. The metabolism of calcium in patients with spinal cord injuries. Ann Surg. 1949;129(2):177-184
10. Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H. Relationship between the duration of paralysis and bone structure: A pQCT study of spinal cord injured individuals. Bone. 2004;34(5):869-880
11. Shields RK, Dudley-Javoroski S. Musculoskeletal plasticity after acute spinal cord injury: Effects of long-term neuromuscular electrical stimulation training. J Neurophysiol. 2006;95(4):2380-2390
12. Shields RK, Dudley-Javoroski S, Boaldin KM, Corey TA, Fog DB, Ruen JM. Peripheral quantitative computed tomography: Measurement sensitivity in persons with and without spinal cord injury. Arch Phys Med Rehabil. 2006; 87(10):1376-1381
13. Keating JF, Kerr M, Delargy M. Minimal trauma causing fractures in patients with spinal cord injury. Disabil Rehabil. 1992;14(2):108-109
14. Shields RK. Fatigability, relaxation properties, and electromyographic responses of the human paralyzed soleus muscle. J Neurophysiol. 1995;73(6):2195-2206.
15. Shields RK, Law LF, Reiling B, Sass K, Wilwert J. Effects of electrically induced fatigue on the twitch and tetanus of paralyzed soleus muscle in humans. J Appl Physiol. 1997;82(5):1499-1507.
16. Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35(2):86-91.
17. Gerrits HL, De Haan A, Hopman MT, Van Der Woude LH, Jones DA, Sargeant AJ. Contractile properties of the quadriceps muscle in individuals with spinal cord injury. Muscle Nerve. 1999;22(9):1249-1256
18. Talmadge RJ, Roy RR, Caiozzo VJ, Edgerton VR. Mechanical properties of rat soleus after long-term spinal cord transection. J Appl Physiol. 2002;93(4):1487-1497
19. Talmadge RJ, Castro MJ, Apple DF Jr, Dudley GA. Phenotypic adaptations in human muscle fibers 6 and 24 wk after spinal cord injury. J Appl Physiol. 2002;92(1):147-154
20. Round JM, Barr FM, Moffat B, Jones DA. Fibre areas and histochemical fibre types in the quadriceps muscle of paraplegic subjects. J Neurol Sci. 1993;116(2):207-211
21. Grimby G, Broberg C, Krotkiewska I, Krotkiewski M. Muscle fiber composition in patients with traumatic cord lesion. Scand J Rehabil Med. 1976;8(1):37-42.
22. Scelsi R, Marchetti C, Poggi P, Lotta S, Lommi G. Muscle fiber type morphology and distribution in paraplegic patients with traumatic cord lesion. Histochemical and ultrastructural aspects of rectus femoris muscle. Acta Neuropathol. 1982;57(4):243-248
23. Chilibeck PD, Jeon J, Weiss C, Bell G, Burnham R. Histochemical changes in muscle of individuals with spinal cord injury following functional electrical stimulated exercise training. Spinal Cord. 1999;37:264-268
24. Otis JS, Roy RR, Edgerton VR, Talmadge RJ. Adaptations in metabolic capacity of rat soleus after paralysis. J Appl Physiol. 2004;96(2):584-596
25. Castro MJ, Apple DF Jr, Staron RS, Campos GE, Dudley GA. Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol. 1999;86(1): 350-358
26. Talmadge RJ, Roy RR, Edgerton VR. Persistence of hybrid fibers in rat soleus after spinal cord transection. Anat Rec. 1999;255(2):188-201.
27. Roy RR, Talmadge RJ, Hodgson JA, Zhong H, Baldwin KM, Edgerton VR. Training effects on soleus of cats spinal cord transected (T12-13) as adults. Muscle Nerve. 1998;21(1):63-71.
28. Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, Kjaer M. Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: Effects of long-term functional electrical stimulation (FES). Pflugers Arch. 1996;431(4):513-518
29. Lieber RL, Friden JO, Hargens AR, Feringa ER. Long-term effects of spinal cord transection on fast and slow rat skeletal muscle. II. Morphometric properties. Exp Neurol. 1986;91(3):435-448
30. Martin TP, Stein RB, Hoeppner PH, Reid DC. Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. J Appl Physiol. 1992; 72(4):1401-1406
31. 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(4):373-378
32. Talmadge RJ. Myosin heavy chain isoform expression following reduced neuromuscular activity: Potential regulatory mechanisms. Muscle Nerve. 2000;23(5):661-679
33. Shields RK, Chang YJ, Dudley-Javoroski S, Lin CH. Predictive model of muscle fatigue after spinal cord injury in humans. Muscle Nerve. 2006;34(1):84-91.
34. Shields RK, Dudley-Javoroski S. Musculoskeletal adaptation in chronic spinal cord injury: Effects of long-term soleus electrical stimulation training. J Neurorehabil Neural Repair. 2007;21(2):169-179
35. Gerrits HL, de Haan A, Sargeant AJ, Dallmeijer A, Hopman MT. Altered contractile properties of the quadriceps muscle in people with spinal cord injury following functional electrical stimulated cycle training. Spinal Cord. 2000;38(4):214-223
36. Mohr T, Andersen JL, Biering-Sorensen F, Galbo H, Bangsbo J, Wagner A, Kjaer M. Long-term adaptation to electrically induced cycle training in severe spinal cord injured individuals. Spinal Cord. 1997;35(1):1-16. Erratum in: Spinal Cord. 1997;35(4):262.
37. Gerrits HL, Hopman MT, Sargeant AJ, Jones DA, De Haan A. Effects of training on contractile properties of paralyzed quadriceps muscle. Muscle Nerve. 2002;25(4): 559-567
38. Hjeltnes N, Aksnes AK, Birkeland KI, Johansen J, Lannem A, Wallberg-Henriksson H. Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients. Am J Physiol. 1997;273(3 Pt 2):R1072-79.
39. Mahoney ET, Bickel CS, Elder C, Black C, Slade JM, Apple DR Jr, Dudley GA. Changes in skeletal muscle size and glucose tolerance with electrically stimulated resistance training in subjects with chronic spinal cord injury. Arch Phys Med Rehabil. 2005;86(7):1502-1504
40. Dudley GA, Castro MJ, Rogers S, Apple DF Jr. A simple means of increasing muscle size after spinal cord injury: A pilot study. Eur J Appl Physiol Occup Physiol. 1999; 80(4):394-396 [PMID: 10483812] (Pubitemid 29405675)
41. Crameri RM, Weston AR, Rutkowski S, Middleton JW, Davis GM, Sutton JR. Effects of electrical stimulation leg training during the acute phase of spinal cord injury: A pilot study. Eur J Appl Physiol. 2000;83(4-3):409-415 [PMID: 11138583] (Pubitemid 32014227)
42. Gerrits HL, Hopman MT, Offringa C, Engelen BG, Sargeant AJ, Jones DA, Haan A. Variability in fibre properties in paralysed human quadriceps muscles and effects of training. Pflugers Arch. 2003;445(6):734-740
43. Crameri RM, Weston A, Climstein M, Davis GM, Sutton JR. Effects of electrical stimulation-induced leg training on skeletal muscle adaptability in spinal cord injury. Scand J Med Sci Sports. 2002;12(5):316-322
44. Kjaer M, Mohr T, Biering-Sorensen F, Bangsbo J. Muscle enzyme adaptation to training and tapering-off in spinal-cord- injured humans. Eur J Appl Physiol. 2001;84(5): 482-486
45. Dupont-Versteegden EE, Houle JD, Gurley CM, Peterson CA. Early changes in muscle fiber size and gene expression in response to spinal cord transection and exercise. Am J Physiol. 1998;275(4 Pt 1):C1124-33.
46. Roy RR, Zhong H, Hodgson JA, Grossman EJ, Siengthai B, Talmadge RJ, Edgerton VR. Influences of electromechanical events in defining skeletal muscle properties. Muscle Nerve. 2002;26(2):238-251
47. Huang RP, Rubin CT, McLeod KJ. Changes in postural muscle dynamics as a function of age. J Gerontol A Biol Sci Med Sci. 1999;54(8):B352-57.
48. Hartkopp A, Harridge SD, Mizuno M, Ratkevicius A, Quistorff B, Kjaer M, Biering-Sorensen F. Effect of training on contractile and metabolic properties of wrist extensors in spinal cord-injured individuals. Muscle Nerve. 2003;27(1):72-80.
49. Crameri RM, Cooper P, Sinclair PJ, Bryant G, Weston A. Effect of load during electrical stimulation training in spinal cord injury. Muscle Nerve. 2004;29(1):104-111
50. Mueller MJ, Maluf KS. Tissue adaptation to physical stress: A proposed "Physical Stress Theory" to guide physical therapist practice, education, and research. Phys Ther. 2002;82(4):383-403.
51. Brown WE, Salmons S, Whalen RG. The sequential replacement of myosin subunit isoforms during muscle type transformation induced by long term electrical stimulation. J Biol Chem. 1983;258(23):14686-14692
52. Gordon T, Tyreman N, Rafuse VF, Munson JB. Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. I. Muscle and motor unit properties. J Neurophysiol. 1997;77(5): 2585-2604.
53. Salmons S, Sreter FA. Significance of impulse activity in the transformation of skeletal muscle type. Nature. 1976; 263(5572):30-34.
54. Sutherland H, Jarvis JC, Kwende MM, Gilroy SJ, Salmons S. The dose-related response of rabbit fast muscle to long-term low-frequency stimulation. Muscle Nerve. 1998; 21(12):1632-1646
55. Shields RK, Dudley-Javoroski S, Cole KR. Feedback-controlled stimulation enhances human paralyzed muscle performance. J Appl Physiol. 2006;101(5):1312-1319
56. Shields RK, Dudley-Javoroski S, Littmann AE. Postfatigue potentiation of paralyzed soleus muscle: Evidence for adaptation with long-term electrical stimulation training. J Appl Physiol. 2006;101(2):556-565
57. Cybulski GR, Penn RD, Jaeger RJ. Lower extremity functional neuromuscular stimulation in cases of spinal cord injury. Neurosurgery. 1984;15(1):132-146
58. Jaeger RJ. Lower extremity applications of functional neuromuscular stimulation. Assist Technol. 1992;4(1):19-30.
59. Yarkony GM, Roth EJ, Cybulski G, Jaeger RJ. Neuromuscular stimulation in spinal cord injury: I: Restoration of functional movement of the extremities. Arch Phys Med Rehabil. 1992;73(1):78-86.
60. Yarkony GM, Jaeger RJ, Roth E, Kralj AR, Quintern J. Functional neuromuscular stimulation for standing after spinal cord injury. Arch Phys Med Rehabil. 1990;71(3): 201-206
61. Billian C, Gorman PH. Upper extremity applications of functional neuromuscular stimulation. Assist Technol. 1992; 4(1):31-39.
62. Goodship AE, Lanyon LE, McFie H. Functional adaptation of bone to increased stress. An experimental study. J Bone Joint Surg Am. 1979;61(4):539-546
63. Kralj AR, Bajd T. Functional electrical stimulation. Standing and walking after spinal cord injury. Boca Raton (FL): CRC Press; 1989.
64. Lu TW, Taylor SJ, O'Connor JJ, Walker PS. Influence of muscle activity on the forces in the femur: An in vivo study. J Biomech. 1997;30(11-12):1101-1106
65. Lanyon LE. Using functional loading to influence bone mass and architecture: Objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone. 1996;18(1 Suppl):37S-43S.
66. Schultheis L. The mechanical control system of bone in weightless spaceflight and in aging. Exp Gerontol. 1991; 26(2-3):203-214
67. Mazess RB, Whedon GD. Immobilization and bone. Calcif Tissue Int. 1983;35(3):265-267
68. Frey-Rindova P, De Bruin ED, Stussi E, Dambacher MA, Dietz V. Bone mineral density in upper and lower extremities during 12 months after spinal cord injury measured by peripheral quantitative computed tomography. Spinal Cord. 2000;38(1):26-32.
69. Bauman WA, Spungen AM, Wang J, Pierson RN Jr, Schwartz E. Continuous loss of bone during chronic immobilization: A monozygotic twin study. Osteoporos Int. 1999;10(2):123-127
70. Slade JM, Bickel CS, Modlesky CM, Majumdar S, Dudley GA. Trabecular bone is more deteriorated in spinal cord injured versus estrogen-free postmenopausal women. Osteoporos Int. 2005;16(5):263-272
71. Modlesky CM, Majumdar S, Narasimhan A, Dudley GA. Trabecular bone microarchitecture is deteriorated in men with spinal cord injury. J Bone Miner Res. 2004;19(1): 48-55.
72. Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA. Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res. 2000;15(1):32-40.
73. Parfitt AM. Trabecular bone architecture in the pathogenesis and prevention of fracture. Am J Med. 1987;82(1B): 68-72.
74. Modlesky CM, Slade JM, Bickel CS, Meyer RA, Dudley GA. Deteriorated geometric structure and strength of the midfemur in men with complete spinal cord injury. Bone. 2005;36(2):331-339
75. De Bruin ED, Herzog R, Rozendal RH, Michel D, Stussi E. Estimation of geometric properties of cortical bone in spinal cord injury. Arch Phys Med Rehabil. 2000;81(2): 150-156
76. Ferretti JL, Capozza RF, Zanchetta JR. Mechanical validation of a tomographic (pQCT) index for noninvasive estimation of rat femur bending strength. Bone. 1996;18(2): 97-102.
77. Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I. Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: A peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone. 2000;27(3):351-357
78. Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet- sports players: A peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res. 2003;18(2):352-359
79. Jamsa T, Jalovaara P, Peng Z, Vaananen HK, Tuukkanen J. Comparison of three-point bending test and peripheral quantitative computed tomography analysis in the evaluation of the strength of mouse femur and tibia. Bone. 1998;23(2): 155-161
80. 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(3):330-335 [PMID: 2114994] (Pubitemid 20189333)
81. Garland DE, Stewart CA, Adkins RH, Hu SS, Rosen C, Liotta FJ, Weinstein DA. Osteoporosis after spinal cord injury. J Orthop Res. 1992;10(3):371-378
82. Uebelhart D, Demiaux-Domenech B, Roth M, Chantraine A. Bone metabolism in spinal cord injured individuals and in others who have prolonged immobilisation. A review. Paraplegia. 1995;33(11):669-673
83. 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(3):498-504.
84. Ragnarsson KT, Sell GH. Lower extremity fractures after spinal cord injury: A retrospective study. Arch Phys Med Rehabil. 1981;62(9):418-423
85. Comarr AE, Hutchinson RH, Bors E. Extremity fractures of patients with spinal cord injuries. Am J Surg. 1962;103: 732-739
86. Eichenholtz SN. Management of long-bone fractures in paraplegic patients. J Bone Joint Surg. 1963;45:299-310.
87. 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(11):790-796
88. Wolff J. Das gesetz der transformation der knochen. Berlin (Germany): Hirschwald; 1892.
89. Wolff J. The law of bone remodeling. New York (NY): Springer-Verlag; 1986.
90. Frost HM. Bone "mass" and the "mechanostat": A proposal. Anat Rec. 1987;219(1):1-9.
91. Frost HM. Skeletal structural adaptations to mechanical usage (SATMU): 1. Redefining Wolff's law: The bone modeling problem. Anat Rec. 1990;226(4):403-413
92. Frost HM. Skeletal structural adaptations to mechanical usage (SATMU): 2. Redefining Wolff's law: The remodeling problem. Anat Rec. 1990;226(4):414-422
93. Frost HM. Bone's mechanostat: A 2003 update. Anat Rec A Discov Mol Cell Evol Biol. 2003;275(2):1081-1101.
94. Lanyon LE. Osteocytes, strain detection, bone modeling and remodeling. Calcif Tissue Int. 1993;53 Suppl 1:S102-7.
95. Ozkaya N, Nordin M. Fundamentals of biomechanics: Equilibrium, motion, and deformation. New York (NY): Springer; 1999.
96. Frost HM. Vital biomechanics: Proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int. 1988;42(3):145-156
97. Heinonen A, Sievanen H, Kyrolainen H, Perttunen J, Kannus P. Mineral mass, size, and estimated mechanical strength of triple jumpers' lower limb. Bone. 2001;29(3): 279-285
98. Nikander R, Sievanen H, Heinonen A, Kannus P. Femoral neck structure in adult female athletes subjected to different loading modalities. J Bone Miner Res. 2005;20(3): 520-528
99. Heinonen A, Sievanen H, Kannus P, Oja P, Vuori I. Site-specific skeletal response to long-term weight training seems to be attributable to principal loading modality: A pQCT study of female weightlifters. Calcif Tissue Int. 2002;70(6):469-474
100. Kanehisa H, Fukunaga T. Profiles of musculoskeletal development in limbs of college Olympic weightlifters and wrestlers. Eur J Appl Physiol Occup Physiol. 1999; 79(5):414-420
101. Mosekilde L. Osteoporosis and exercise. Bone. 1995; 17(3):193-195
102. Frost HM. The role of changes in mechanical usage set points in the pathogenesis of osteoporosis. J Bone Miner Res. 1992;7(3):253-261
103. Rubin C, Gross T, Qin YX, Fritton S, Guilak F, McLeod K. Differentiation of the bone-tissue remodeling response to axial and torsional loading in the turkey ulna. J Bone Joint Surg Am. 1996;78(10):1523-1533
104. Jarvinen TL, Kannus P, Sievanen H, Jolma P, Heinonen A, Jarvinen M. Randomized controlled study of effects of sudden impact loading on rat femur. J Bone Miner Res. 1998;13(9):1475-1482
105. Chow JW, Jagger CJ, Chambers TJ. Characterization of osteogenic response to mechanical stimulation in cancellous bone of rat caudal vertebrae. Am J Physiol. 1993; 265(2 Pt 1):E340-47.
106. Mosley JR, March BM, Lynch J, Lanyon LE. Strain magnitude related changes in whole bone architecture in growing rats. Bone. 1997;20(3):191-198
107. Lee KC, Maxwell A, Lanyon LE. Validation of a technique for studying functional adaptation of the mouse ulna in response to mechanical loading. Bone. 2002;31(3):407-412
108. Mosley JR, Lanyon LE. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone. 1998;23(4): 313-318
109. Robling AG, Hinant FM, Burr DB, Turner CH. Shorter, more frequent mechanical loading sessions enhance bone mass. Med Sci Sports Exerc. 2002;34(2):196-202.
110. Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH. Mechanical loading of diaphyseal bone in vivo: The strain threshold for an osteogenic response varies with location. J Bone Miner Res. 2001;16(12):2291-2297
111. De Souza RL, Matsuura M, Eckstein F, Rawlinson SC, Lanyon LE, Pitsillides AA. Non-invasive axial loading of mouse tibiae increases cortical bone formation and modifies trabecular organization: A new model to study cortical and cancellous compartments in a single loaded element. Bone. 2005;37(16):810-818
112. Rubin C, Judex S, Qin YX. Low-level mechanical signals and their potential as a non-pharmacological intervention for osteoporosis. Age Ageing. 2006;35 Suppl 2:ii32-ii36.
113. Rubin C, Turner AS, Mallinckrodt C, Jerome C, McLeod K, Bain S. Mechanical strain, induced noninvasively in the high-frequency domain, is anabolic to cancellous bone, but not cortical bone. Bone. 2002;30(3):445-452 [PMID: 11882457] (Pubitemid 34204118)
114. Bloomfield SA, Allen MR, Hogan HA, Delp MD. Site- and compartment-specific changes in bone with hindlimb unloading in mature adult rats. Bone. 2002;31(1):149-157
115. Allen MR, Bloomfield SA. Hindlimb unloading has a greater effect on cortical compared with cancellous bone in mature female rats. J Appl Physiol. 2003;94(2):642-650
116. David V, Lafage-Proust MH, Laroche N, Christian A, Ruegsegger P, Vico L. Two-week longitudinal survey of bone architecture alteration in the hindlimb-unloaded rat model of bone loss: Sex differences. Am J Physiol Endocrinol Metab. 2006;290(3):E440-47. [PMID: 16467486] (Pubitemid 43671689)
117. Zhang Y, Ji SR, Wu CY, Fan XH, Zhou HJ, Liu GL. Observation of locomotor functional recovery in adult complete spinal rats with BWSTT using semiquantitative and qualitative methods. Spinal Cord. 2007;45(7):496-501.
118. Muir GD. Locomotor plasticity after spinal injury in the chick. J Neurotrauma. 1999;16(8):705-711
119. De Leon RD, Hodgson JA, Roy RR, Edgerton VR. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol. 1998;79(3):1329-1340
120. Saunders NR, Kitchener P, Knott GW, Nicholls JG, Potter A, Smith TJ. Development of walking, swimming and neuronal connections after complete spinal cord transection in the neonatal opossum, Monodelphis domestica. J Neurosci. 1998;18(1):339-355
121. Fluckey JD, Dupont-Versteegden EE, Montague DC, Knox M, Tesch P, Peterson CA, Gaddy-Kurten D. A rat resistance exercise regimen attenuates losses of musculoskeletal mass during hindlimb suspension. Acta Physiol Scand. 2002;176(4):293-300.
122. Kunkel CF, Scremin AM, Eisenberg B, Garcia JF, Roberts S, Martinez S. Effect of "standing" on spasticity, contracture, and osteoporosis in paralyzed males. Arch Phys Med Rehabil. 1993;74(1):73-78.
123. Needham-Shropshire BM, Broton JG, Klose KJ, Lebwohl N, Guest RS, Jacobs PL. Evaluation 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. 1997;78(8):799-803.
124. Thoumie P, Le Claire G, Beillot J, Dassonville J, Chevalier T, Perrouin-Verbe B, Bedoiseau M, Busnel M, Cormerais A, Courtillon A. Restoration of functional gait in paraplegic patients with the RGO-II hybrid orthosis. A multicenter controlled study. II: Physiological evaluation. Paraplegia. 1995;33(11):654-659
125. Leeds EM, Klose KJ, Ganz W, Serafini A, Green BA. Bone mineral density after bicycle ergometry training. Arch Phys Med Rehabil. 1990;71(3):207-209
126. BeDell KK, Scremin AM, Perell KL, Kunkel CF. Effects of functional electrical stimulation-induced lower extremity cycling on bone density of spinal cord-injured patients. Am J Phys Med Rehabil. 1996;75(1):29-34.
127. Snyder WS. Report of the task group on reference man. Oxford (England): Pergamon; 1975.
128. Bloomfield SA, Mysiw WJ, Jackson RD. Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone. 1996;19(1):61-68.
129. Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M. Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int. 1997;61(1):22-25.
130. Shields RK, Dudley-Javoroski S, Law LA. Electrically induced muscle contractions influence bone density decline after spinal cord injury. Spine. 2006;31(5):548-553
131. Granhed H, Jonson R, Hansson T. The loads on the lumbar spine during extreme weight lifting. Spine. 1987;12(2): 146-149
132. Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: Spatial uniformity and self-similarity of low-magnitude strains. J Biomech. 2000;33(3):317-325
133. Serre CM, Farlay D, Delmas PD, Chenu C. Evidence for a dense and intimate innervation of the bone tissue, including glutamate-containing fibers. Bone. 1999;25(6):623-629 [PMID: 10593406] (Pubitemid 29525427)
134. Ivanusic JJ, Mahns DA, Sahai V, Rowe MJ. Absence of large-diameter sensory fibres in a nerve to the cat humerus. J Anat. 2006;208(2):251-255
135. Konttinen Y, Imai S, Suda A. Neuropeptides and the puzzle of bone remodeling. State of the art. Acta Orthop Scand. 1996;67(6):632-639
136. Bjurholm A, Kreicbergs A, Brodin E, Schultzberg M. Substance P- and CGRP-immunoreactive nerves in bone. Peptides. 1988;9(1):165-171
137. Garcia-Castellano JM, Diaz-Herrera P, Morcuende JA. Is bone a target-tissue for the nervous system? New advances on the understanding of their interactions. Iowa Orthop J. 2000;20:49-58.
138. Chantraine A, van Ouwenaller C, Hachen HJ, Schinas P. Intra-medullary pressure and intra-osseous phlebography in paraplegia. Paraplegia. 1979;17(4):391-399
139. Chantraine A. Actual concept of osteoporosis in paraplegia. Paraplegia. 1978;16(1):51-58.
140. Dupont-Versteegden EE, Houle JD, Dennis RA, Zhang J, Knox M, Wagoner G, Peterson CA. Exercise-induced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve. 2004; 29(1):73-81.
141. Henderson CE, Phillips HS, Polluck RA, Davies AM, Lemeulle C, Armanini M, Simmons L, Moffet B, Vandlen RA, Simpson LC. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science. 1994;266(5187):1062-64. [PMID: 7973664] Erratum in: Science. 1995;267(5199):777. (Pubitemid 24373728)
142. Snider WD, Lichtman JW. Are neurotrophins synaptotrophins? Mol Cell Neurosci. 1996;7(6):433-442
143. DiStefano PS, Friedman B, Radziejewski C, Alexander C, Boland P, Schick CM, Lindsay RM, Wiegand SJ. The neurotrophins BDNF, NT-3, and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron. 1992;8(5):983-993
144. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron. 1993;10(3):359-367
145. Gomez-Pinilla F, Ying Z, Opazo P, Roy RR, Edgerton VR. Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci. 2001; 13(6):1078-1084
146. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P. Neural adaptation to resistance training: Changes in evoked V-wave and H-reflex responses. J Appl Physiol. 2002;92(6):2309-2318
147. Sale DG, MacDougall JD, Upton AR, McComas AJ. Effect of strength training upon motoneuron excitability in man. Med Sci Sports Exerc. 1983;15(1):57-62.
148. Skinner RD, Houle JD, Reese NB, Berry CL, Garcia-Rill E. Effects of exercise and fetal spinal cord implants on the H-reflex in chronically spinalized adult rats. Brain Res. 1996;729(1):127-131
149. Trimble MH, Du P, Brunt D, Thompson FJ. Modulation of triceps surae H-reflexes as a function of the reflex activation history during standing and stepping. Brain Res. 2000;858(2):274-283