Heterotopic ossification following traumatic brain injury and spinal cord injury: Insight into the etiology and pathophysiology

Journal of Musculoskeletal Neuronal Interactions

Volumn 12, Issue 4, 2012, Pages 230-240

  Sakellariou, V I ^a   Grigoriou, E ^a   Mavrogenis, A F ^a   Soucacos, P N ^a   Papagelopoulos, P J ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Brain injury; Heterotopic; Ossification; TBI; Trauma

Indexed keywords

ALKALINE PHOSPHATASE; BISPHOSPHONIC ACID DERIVATIVE; BONE MORPHOGENETIC PROTEIN; C REACTIVE PROTEIN; ETIDRONIC ACID; FIBROBLAST GROWTH FACTOR 2; HLA ANTIGEN; INDOMETACIN; INTERLEUKIN 6; LEPTIN; MATRIX METALLOPROTEINASE; NONSTEROID ANTIINFLAMMATORY AGENT; PARATHYROID HORMONE; PLACEBO; ROFECOXIB; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; WNT PROTEIN;

ARTICLE; ARTIFICIAL VENTILATION; AUTONOMIC DYSFUNCTION; BONE DEVELOPMENT; BONE TURNOVER; COMA; DEMOGRAPHY; ELECTROMAGNETIC FIELD; ENVIRONMENTAL FACTOR; EVIDENCE BASED MEDICINE; GENE MUTATION; GENETIC PREDISPOSITION; HETEROTOPIC OSSIFICATION; HUMAN; IMMUNOPATHOLOGY; INFLAMMATION; MUSCLE HYPERTONIA; ORTHOPEDIC SURGERY; OSSIFYING MYOSITIS; OSTEOPROGENITOR CELL; PATHOPHYSIOLOGY; PHYSIOTHERAPY; PROGNOSIS; RANGE OF MOTION; RISK FACTOR; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SPASTICITY; SPINAL CORD INJURY; STEM CELL; TRAUMATIC BRAIN INJURY; TREATMENT DURATION;

ANIMALS; BONE AND BONES; BRAIN INJURIES; HUMANS; OSSIFICATION, HETEROTOPIC; SPINAL CORD INJURIES;

EID: 84870795658     PISSN: 11087161     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (101)

1. Cope R. Heterotopic ossification. South Med J 1990; 83:1058-1064.
2. Ekelund A, Brosjo O, Nilsson OS. Experimental induction of heterotopic bone. Clin Orthop Relat Res 1991; 263:102-112.
3. Citta-Pietrolungo TJ, Alexander MA, Steg NL. Early detection of heterotopic ossification in young patients with traumatic brain injury. Arch Phys Med Rehabil 1992; 73:258-262.
4. Garland DE. Clinical observations on fractures and heterotopic ossification in the spinal cord and traumatic brain injured populations. Clin Orthop Relat Res 1988;233:86-101.
5. Garland DE. A clinical perspective on common forms of acquired heterotopic ossification. Clin Orthop Relat Res 1991;263:13-29.
6. Van Kuijk AA, Geurts AC, van Kuppevelt HJ. Neurogenic heterotopic ossification in spinal cord injury. Spinal Cord 2002;40:313-326.
7. Bidner SM, Rubins IM, Desjardins JV, et al. Evidence for a humoral mechanism for enhanced osteogenesis after head injury. J Bone Joint Surg Am 1990;72:1144-149.
8. Brighton CT, Hunt RM. Early histologic and ultrastructural changes in microvessels of periosteal callus. J Orthop Trauma 1997;11:244-253.
9. Chalmers J, Gray DH, Rush J. Observations on the induction of bone in soft tissues. J Bone Joint Surg Br 1975; 57:36-45.
10. Marusic A, Katavic V, Grcevic D, Lukic IK. Genetic variability of new bone induction in mice. Bone 1999;25:25-32.
11. Boes M, Kain M, Kakar S, Nicholls F, Cullinane D, Gerstenfeld L, Einhorn TA, Tornetta P. Osteogenic effects of traumatic brain injury on experimental fracture- healing. J Bone Joint Surg Am 2006;88:738-743. Erratum in: J Bone Joint Surg Am 2006;88:1602.
12. Cadosch D, Gautschi OP, Thyer M, Song S, Skirving AP, Filgueira L, Zellweger R. Humoral factors enhance fracture- healing and callus formation in patients with traumatic brain injury. J Bone Joint Surg Am 2009;91:282-288. Erratum in: J Bone Joint Surg Am 2009;91:938.
13. Gautschi OP, Cadosch D, Frey SP, Skirving AP, Filgueira L, Zellweger R. Serum-mediated osteogenic effect in traumatic brain-injured patients. ANZ J Surg 2009; 79:449-455.
14. Kurer MH, Khoker MA, Dandona P. Human osteoblast stimulation by sera from paraplegic patients with heterotopic ossification. Paraplegia 1992;30:165-168.
15. Gautschi OP, Toffoli AM, Joesbury KA et al. Osteoinductive effect of cerebrospinal fluid from brain-injured patients. J. Neurotrauma 2007;24:154-162.
16. Mitchell EJ, Canter J, Norris P, Jenkins J, Morris J. The genetics of heterotopic ossification: insight into the bone remodeling pathway. J Orthop Trauma 2010;24(9):530-533.
17. Ritter MA, Vaughan RB. Ectopic ossification after total hip arthroplasty. Predisposing factors, frequency, and effect on results. J Bone Joint Surg Am 1977;59:345-351.
18. Ahrengart L. Periarticular heterotopic ossification after total hip arthroplasty. Risk factors and consequences. Clin Orthop 1991;263:49-58.
19. Wittenberg RH, Peschke U, Bötel U. Heterotopic ossification after spinal cord injury: Epidemiology and risk factors. J Bone Joint Surg Br 1992;74:215-218.
20. Kewalramani LS. Ectopic ossification. Am J Phys Med 1977;56:99-121.
21. Scher AT. The incidence of ectopic bone formation in post-traumatic paraplegic patients of different racial groups. Paraplegia 1976;14:202-206.
22. Larson JM, Michalski JP, Collacott MJ, Eltorai EA, Mc-Combs CC, Madorsky JB. Increased prevalence of HLA-B27 in 19. patients with ectopic ossification following traumatic spinal cord injury. Rheumatol Rehabil 1981;20:193-197.
23. Garland DE, Alday B, Vernos KG. Heterotopic ossification and HLA antigens. Arch Phys Med Rehabil 1984; 65:531-532.
24. Weiss S, Garland Z, Ohri A, Mizrachi Y, Orgad S, Efter T, et al. Histo compatibility (HLA) antigens in heterotopic ossification associated with neurological injury. J Rheumatol 1979;6:88-91.
25. Hunter T, Dubo HI, Hildahl CR, Smith NJ, Schroeder ML. Histocompatibility antigens in patients with spinal cord injury or cerebral damage complicated by heterotopic ossification. Rheumatol Rehabil 1980;19:97-99.
26. Jaimo AHN, De La Pena LS, Shore EM, Kaplan FS. Paresis of a bone morphogenetic protein-antagonist response in a genetic disorder of heterotopic ossification. J Bone Joint Surg 2003;85:667-674.
27. Kaplan FS, Glaser DL, Hebela N, Shore EM: Heterotopic ossification. J Am Acad Orthop Surg 2004;12:116-125.
28. Feldman G, Li M, Martin S, et al. Fibrodysplasia ossificans progressiva, a heritable disorder of severe heterotopic ossification, maps to human chromosome 4q27-31. Am J Hum Genet 2000;66:128-35.
29. Shore EM, Xu M, Feldman GJ, et al. A recurrent mutation in the BMP type I receptor ACVR1 causes inherited and poradic fibrodysplasia ossificans progressiva. Nat Genet 2006;38:525-752.
30. De Lee J, Ferrari A, Charnley J. Ectopic bone formation following low friction arthroplasty of the hip. Clin Orthop 1976;121:53-59.
31. Sundaram NA, Murphy JC. Heterotopic bone formation following total hip arthroplasty in ankylosing spondylitis. Clin Orthop Relat Res 1986;207:223-226.
32. Elefteriou F. Neuronal signaling and the regulation of bone remodeling. Cell Mol Life Sci 2005;62:2339-2349.
33. Takeda S, Elefteriou F, Levasseur R, et al. Leptin regulates bone formation via the sympathetic nervous system. Cell 2002;111:305-317.
34. Garland DE, O'Hollaren RM. Fractures and dislocations about the elbow in the head-injured adult. Clin Orthop Relat Res 1982;168:38-41.
35. Pape HC, Lehmann U, van Griensven M, Gänsslen A, von Glinski S, Krettek C.Heterotopic ossifications in patients after severe blunt trauma with and without head trauma: incidence and patterns of distribution. J Orthop Trauma 2001;15(4):229-237.
36. Michelsson JE, Rauschning W. Pathogenesis of experimental heterotopic bone formation following temporary forcible exercising of immobilized limbs. Clin Orthop 1983;176:265-272.
37. Michelsson JE, Ganroth G, Andersson LC. Myositis ossificans following forcible manipulation of the leg. A rabbit model for the study of heterotopic bone formation. J Bone Joint Surg 1980;62:811-815.
38. Bartlett CS, Rapuano BE, Lorich DG, Wu T, Anderson RC, Tomin E, Hsu JF, Lane JM, Helfet DL. Early changes in prostaglandins precede bone formation in a rabbit model of heterotopic ossification. Bone 2006;38(3):322-332.
39. Casavant AM, Hastings H. Heterotopic ossification about the elbow: a therapist's guide to evaluation and management. J Hand Ther 2006;19(2):255-266.
40. Brighton CT, Schaffer JL, Shapiro DB, et al. Proliferation and macromolecular synthesis by rat calvarial bone cells grown in various oxygen tensions. J Bone Joint Surg Am 1991;9:847-854.
41. Boulet M, Marier JR. Precipitation of calcium phosphates from solution at near physiological concentration. Arch Biochem 1961;93:157.
42. Newman RJ, Stone MH, Mukherjee SK. Accelerated fracture union in association with severe head injury. Injury 1987; 18:241-246.
43. Da Paz AC, Carod Artal FJ, Kalil RK. The function of propioceptors in bone organization: a possible explanation for neurogenic heterotopic ossifica- tion in patients with neurological damage. Med Hypotheses 2007;68:67-73.
44. McCarthy EF, Sundaram M. Heterotopic ossification: a review. Skeletal Radiol 2005;34:609-619.
45. Vanden Bossche L, Vanderstraeten G. Heterotopic ossification: a review. J Rehabil Med 2005;37:129-136.
46. Tsur A, Sazbon L, Lotem M. Relationship between muscular tone, movement and periarticular new bone formation in postcoma-unaware (PC-U) patients. Brain Inj 1996;10:259-262.
47. Cadosch D, Toffoli AM, Gautschi OP, Frey SP, Zellweger R, Skirving AP, Filgueira L. Serum after traumatic brain injury increases proliferation and supports expression of osteoblast markers in muscle cells. J Bone Joint Surg Am 2010;92(3):645-653.
48. Potter BK, Forsberg JA, Davis TA, Evans KN, Hawksworth JS, Tadaki D, Brown TS, Crane NJ, Burns TC, O'Brien FP, Elster EA. Heterotopic ossification following combat-related trauma. J Bone Joint Surg Am 2010;92(Suppl.2):74-89.
49. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006;119:2204-213.
50. Williams JT, Southerland SS, Souza J, Calcutt AF, Cartledge RG. Cells isolated from adult human skeletal muscle capable of differentiating into multiple meso- dermal phenotypes. Am Surg 1999;65:22-26.
51. Mastrogiacomo M, Derubeis AR, Cancedda R. Bone and cartilage formation by skeletal muscle derived cells. J Cell Physiol 2005;204:594-603.
52. Major P, Resnick D, Greenway G. Heterotopic ossification in paraplegia: a possible disturbance of the paravertebral venous plexus. Radiology 1980;136:797-799.
53. Linan E, O'Dell MW, Pierce JM. Continuous passive motion in the management of heterotopic ossification in a brain injured patient. Am J Phys Med Rehabil 2001;80:614-617.
54. Gospodarowicz D, Bialecki H, Greenburg G. Purification of the fibroblast growth factor from bovine brain. J Biol Chem 1987;253:3736-3743.
55. Wildburger R, Zarkovic N, Petek W, et al. Hyper trophic callus formation and craniocerebral trauma: early diagnosis and behavior of basic fibroblast growth factor. Unfallchirurg 1996;99:17-23.
56. Goris RJA, Boekhorst TPA, Nuytinck JKS, et al. Multiple organ failure: generalized autodestructive inflammation? Arch Surg 1985;120:1109-1115.
57. Knauer DJ, Smith GL. Inhibition of biological activity of multi- plication stimulating activity by binding to its carrier protein. Proc Nat Acad Sci 1982;77:7252-7256.
58. Wildburger R, Zarkovic N, Egger G, et al. Comparison of the values of basic fibroblast growth factor determined by an immunoassay in the sera of patients with traumatic brain injury and enhanced osteogenesis and the effects of the same sera on the fibroblast growth in vitro. Eur J Clin Chem Clin Biochem 1995;33:693-698.
59. Falsetti P, Acciai C, Palilla R, Carpinteri F, Patrizio C, Lenzi L. Bedside ultrasound in early diagnosis of neurogenic heterotopic ossification in patients with acquired brain injury. Clin Neurol Neurosurg 2011;113(1):22-27.
60. Arosarena O, Collins W. Comparison of BMP-2 and -4 for rat mandibular bone regeneration at various doses. Orthod. Craniofa Res 2005;8:267-276.
61. Castillo J, Rodríguez I. Biochemical changes and inflammatory response as markers for brain ischaemia: molecular markers of diagnostic utility and prognosis in human clinical practice. Cerebrovasc Dis 2004;17(Suppl.1):7-18.
62. Finfer SR, Cohen J. Severe traumatic brain injury.Resuscitation 2001;48(1):77-90.
63. Crespo AR, Da Rocha AB, Jotz GP, Schneider RF, Grivicich I, Pinheiro K, et al. Increased serum sFas and TNFalpha following isolated severe head injury in males. Brain Inj 2007;21(4):441-447.
64. Steppan CM, Crawford T, Chidsey-Frink KL, Ke HZ, Swick AG. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept 2000;92:73-78.
65. Gordeladze JO, Drevon CA, Syversen U, Reseland JE. Leptin stimulates human osteoblastic formation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis and osteoclastic signaling. J Cell Biochem 2002;85:825-836.
66. Trentz OA, Handschin AE, Bestmann L, Hoerstrup SP, Trentz OL, Platz A. Influence of brain injury on early posttraumatic bone metabolism. Crit Care Med 2005; 33(2):399-406.
67. Ducy P. Cbfa1: A molecular switch in osteoblast biology. Dev Dyn 2000;219:461-471.
68. Ducy P, Desbois C, Boyce B, et al. Increased bone formation in osteocalcin-deficient mice. Nature 1996; 382:448-452.
69. Chenu C, Colucci S, Grano M, et al. Osteocalcin induces chemotaxis, secretion of matrix proteins, and calciummediated intracellular signaling in human osteoclast-like cells. J Cell Biol 1994;127:1149-1158.
70. Takahashi M, Naitou K, Ohishi T, et al. Comparison of biochemical markers of bone turn- over and bone mineral density between hip fracture and vertebral fracture. J Clin Densi tom 2003;6:211-218.
71. Tanigushi T, Matsumoto T, Shindo H. Changes of serum levels of osteocalcin, alkaline phosphatase, IGF-1 and IGF-binding protein-3 during fracture healing. Injury Int J Care 2003; 34:477-479
72. Banse X, Devogelaer JP, Lafosse A, et al. Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 2002;31:70-76.
73. Miyakawa M, Tsushima T, Demura H. Car- boxy-terminal propeptide of type 1 procollagen (PICP) and carboxyterminal telopeptide of type 1 collagen (ICTP) as sensitive markers of bone metabolism in thyroid disease. En- docr J 1996;43:701-708.
74. Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins. Growth Factors 2004;22(4):233-41.
75. Kang Q, Sun MH, Cheng H, Peng Y, Montag AG, Deyrup AT, Jiang W, Luu HH, Luo J, Szatkowski JP, Vanichakarn P, Park JY, Li Y, Haydon RC, He TC. Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adenovirus-mediated gene delivery. Gene Ther 2004;11(17):1312-1320.
76. rd ed. Saunders WB; 2000. p. 19-22.
77. Wildburger R, Zarkovic N, Egger G, Petek W, Zarkovic K, Hofer HP. Basic fibroblast growth factor (BFGF) immunoreactivity as a possible link between head injury and impaired bone fracture healing. Bone Miner 1994;27:183-192.
78. OLIVEIRA, Carla Oliveira de; IKUTA, Nilo and REGNER, Andrea. Outcome biomarkers following severe traumatic brain injury. Rev. bras. ter. intensiva [online]. 2008, vol.20, n.4, pp. 411-421. ISSN 0103-507X.
79. Suehiro E, Fujisawa H, Akimura T, Ishihara H, Kajiwara K, Kato S, et al. Increased matrix metalloproteinase-9 in blood in association with activation of interleukin-6 after traumatic brain injury: influence of hypothermic therapy. J Neurotrauma 2004;21(12):1706-1711.
80. Issack PS, Helfet DL, Lane JM. Role of Wnt signaling in bone remodeling and repair. HSS J 2008;4(1):66-70.
81. Mysiw WJ, Tan J, Jackson RD. Heterotopic ossification. The utility of osteocalcin in diagnosis and management. Am J Phys Med Rehabil 1993;72:184-187.
82. Blackwell KA, Raisz LG, Pilbeam CC. Prostaglandins in bone: bad cop, good cop? Trends Endocrinol Metab 2010; 21(5):294-301.
83. Shehab D, Elgazzar AH, Collier BD. Heterotopic ossification. J Nucl Med 2002;43:346-353.
84. Laurnen EL, Kelly PJ. Blood flow, oxygen consumption, carbon-dioxide production, and blood calcium and pH changes in tibial fractures in dogs. J Bone Joint Surg Am 1969;51:298-308.
85. Brighton CT, Krebs AG. Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg Am 1972;54:323-332.
86. Clements NC, Camilli AE. Heterotopic ossification complicating critical illness. Chest 1993;104:1526-1528.
87. Ellerin BE, Helfat D, Parikh S, et al. Current therapy in the management of heterotopic ossification of the elbow. Am J Phys Med Rehab 1999;78:259-271.
88. Schulze M, Lobenhoffer HP. Heterotopic ossifications of 5 large body joints after 105 days of intensive care with 72 days of artificial ventilation. Unfallchirurg 1997;100(10):839-844.
89. Banovac K, Williams JM, Patrick LD, Haniff YM. Prevention of heterotopic ossification after spinal cord injury with indomethacin. Spinal Cord 2001;39:370-374. [PubMed: 11464310] transplantation and 72 days of artificial ventilation. Unfallchirurg 1997;100:839-844.
90. Banovac K, Gonzalez F, Wade N, Bowker JJ. Intravenous disodium etidronate therapy in spinal cord injury patients with heterotopic ossification. Paraplegia 1993;31:660-666.
91. Spielman G, Gennarelli TA, Rogers CR. Disodium etidronate: its role in preventing heterotopic ossification in severe head injury. Arch Phys Med Rehabil 1983; 64:539-542.
92. Banovac K, Gonzalez F. Evaluation and management of heterotopic ossification in patients with spinal cord injury. Spinal Cord 1997;35:158-162.
93. Banovac K. The effect of etidronate on late development of heterotopic ossification after spinal cord injury. J Spinal Cord Med 2000;23:40-44.
94. Garland DE, Alday B, Venos KG, Vogt JC. Diphosphonate treatment for heterotopic ossification in spinal cord injury patients. Clin Orthop Relat Res 1983:197-200.
95. Melamed E, Robinson D, Halperin N, Wallach N, Keren O, Groswasser Z. Brain injury-related heterotopic bone formation: treatment strategy and results. Am J Phys Med Rehabil 2002;81:670-674.
96. Sautter-Bihl ML, Hultenschmidt B, Liebermeister E, Nanassy A. Fractionated and single-dose radiotherapy for heterotopic bone formation in patients with spinal cord injury. A phase-I/II study. Strahlenther Onkol 2001;177:200-205.
97. Sautter-Bihl ML, Liebermeister E, Nanassy A. Radiotherapy as a local treatment option for heterotopic ossifications in patients with spinal cord injury. Spinal Cord 2000; 38:33-36.
98. Fuller DA, Mark A, Keenan MA. Excision of heterotopic ossification from the knee: a functional outcome study. Clin Orthop Relat Res 2005;438:197-203.
99. Moore TJ. Functional outcome following surgical excision of heterotopic ossification in patients with traumatic brain injury. J Orthop Trauma 1993;7:11-714.
100. de Palma L, Rapali S, Paladini P, Ventura A. Elbow heterotopic ossification in head-trauma patients: diagnosis and treatment. Orthopedics 2002;25:665-668.
101. Lazarus MD, Guttmann D, Rich CE, Keenan MAE. Heterotopic ossification resection about the elbow. Neuro Rehabilitation 1999;12:145-153.