A unilateral cervical spinal cord contusion injury model in non-human primates (Macaca mulatta)

Journal of Neurotrauma

Volumn 33, Issue 5, 2016, Pages 439-459

  Salegio, Ernesto A ^a   Bresnahan, Jacqueline C ^a   Sparrey, Carolyn J ^b   Camisa, William ^c   Fischer, Jason ^c   Leasure, Jeremi ^c   Buckley, Jennifer ^d   Nout Lomas, Yvette S ^e   Rosenzweig, Ephron S ^f,g   Moseanko, Rod ^h   Strand, Sarah ^h   Hawbecker, Stephanie ^h   Lemoy, Marie Josee ^h   Haefeli, Jenny ^a   Ma, Xiaokui ^a   Nielson, Jessica L ^a   Edgerton, V R ⁱ   Ferguson, Adam R ^a   Tuszynski, Mark H ^f,g   Beattie, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

^c ST MARY S MEDICAL CENTER   (United States)

^d UNIVERSITY OF DELAWARE   (United States)

^e Veterinary Dentistry and Oral Surgery   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

biomechanics of injury; contusion; functional recovery; primate; spinal cord injury

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BIOMECHANICS; CEREBROSPINAL FLUID; CERVICAL SPINAL CORD INJURY; CLIMBING; CONTROLLED STUDY; CONTUSION; DISEASE MODEL; EXERCISE; HAND FUNCTION; HISTOLOGY; IMAGE QUALITY; LAMINECTOMY; LOCOMOTION; MALE; MOTOR PERFORMANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OBJECT MANIPULATION; RAT; RHESUS MONKEY; STEREOTACTIC DEVICE; TASK PERFORMANCE; TISSUE SECTION; ANIMAL; CERVICAL VERTEBRA; CONTUSIONS; PATHOLOGY; SPINAL CORD INJURIES;

ANIMALS; CERVICAL VERTEBRAE; CONTUSIONS; DISEASE MODELS, ANIMAL; MACACA MULATTA; MALE; SPINAL CORD INJURIES;

EID: 84959208270     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2015.3956     Document Type: Article

References (66)

1. Geissler, S.A., Schmidt, C.E., and Schallert, T. (2013). Rodent models and behavioral outcomes of cervical spinal cord injury. J. Spine Suppl. 4, 001
2. Streijger, F., Beernink, T.M., Lee, J.H., Bhatnagar, T., Park, S., Kwon, B.K., and Tetzlaff, W. (2013). Characterization of a cervical spinal cord hemicontusion injury in mice using the infinite horizon impactor. J. Neurotrauma 30, 869-883
3. Lee, J.H., Streijger, F., Tigchelaar, S., Maloon, M., Liu, J., Tetzlaff, W., and Kwon, B.K. (2012) A contusive model of unilateral cervical spinal cord injury using the infinite horizon impactor. J. Vis. Exp. 65, 3313
4. Russell, C.M., Choo, A.M., Tetzlaff, W., Chung, T.E., and Oxland, T.R. (2012). Maximum principal strain correlates with spinal cord tissue damage in contusion and dislocation injuries in the rat cervical spine. J. Neurotrauma 29, 1574-1585
5. Anderson, K.D., Sharp, K.G., and Steward, O. (2009). Bilateral cervical contusion spinal cord injury in rats. Exp. Neurol. 220, 9-22
6. Dunham, K.A., Siriphorn, A., Chompoopong, S., and Floyd, C.L. (2010). Characterization of a graded cervical hemicontusion spinal cord injury model in adult male rats. J. Neurotrauma 27, 2091-2106
7. Gensel, J.C., Tovar, C.A., Hamers, F.P., Deibert, R.J., Beattie, M.S., and Bresnahan, J.C. (2006). Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J. Neurotrauma 23, 36-54
8. Tator, C.H. (2006). Review of treatment trials in human spinal cord injury: issues, difficulties, and recommendations. Neurosurgery 59, 957-982
9. Courtine, G., Bunge, M.B., Fawcett, J.W., Grossman, R.G., Kaas, J.H., Lemon, R., Maier, I., Martin, J., Nudo, R.J., Ramon-Cueto, A., Rouiller, E.M., Schnell, L., Wannier, T., Schwab, M.E., and Edgerton, V.R. (2007). Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humans?. Nat. Med. 13, 561-566
10. Kwon, B.K., Ghag, A., Reichl, L., Dvorak, M.F., Illes, J., and Tetzlaff, W. (2012). Opinions on the preclinical evaluation of novel therapies for spinal cord injury: a comparison between researchers and spinal cord-injured individuals. J. Neurotrauma 29, 2367-2374
11. Rosenzweig, E.S., Courtine, G., Jindrich, D.L., Brock, J.H., Ferguson, A.R., Strand, S.C., Nout, Y.S., Roy, R.R., Miller, D.M., Beattie, M.S., Havton, L.A., Bresnahan, J.C., Edgerton, V.R., and Tuszynski, M.H. (2010). Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat. Neurosci. 13, 1505-1510
12. Nout, Y.S., Ferguson, A.R., Strand, S.C., Moseanko, R., Hawbecker, S., Zdunowski, S., Nielson, J.L., Roy, R.R., Zhong, H., Rosenzweig, E.S., Brock, J.H., Courtine, G., Edgerton, V.R., Tuszynski, M.H., Beattie, M.S., and Bresnahan, J.C. (2012). Methods for functional assessment after C7 spinal cord hemisection in the rhesus monkey. Neurorehabil. Neural Repair 26, 556-569
13. Nout, Y.S., Rosenzweig, E.S., Brock, J.H., Strand, S.C., Moseanko, R., Hawbecker, S., Zdunowski, S., Nielson, J.L., Roy, R.R., Courtine, G., Ferguson, A.R., Edgerton, V.R., Beattie, M.S., Bresnahan, J.C., and Tuszynski, M.H. (2012). Animal models of neurologic disorders: a nonhuman primate model of spinal cord injury. Neurotherapeutics 9, 380-392
14. Ferguson, A.R., Irvine, K.A., Gensel, J.C., Nielson, J.L., Lin, A., Ly, J., Segal, M.R., Ratan, R.R., Bresnahan, J.C., and Beattie, M.S. (2013). Derivation of multivariate syndromic outcome metrics for consistent testing across multiple models of cervical spinal cord injury in rats. PloS One 8, e59712
15. Nout, Y.S., Mihai, G., Tovar, C.A., Schmalbrock, P., Bresnahan, J.C., and Beattie, M.S. (2009). Hypertonic saline attenuates cord swelling and edema in experimental spinal cord injury: a study utilizing magnetic resonance imaging. Crit. Care Med. 37, 2160-2166
16. Mihai, G., Nout, Y.S., Tovar, C.A., Miller, B.A., Schmalbrock, P., Bresnahan, J.C., and Beattie, M.S. (2008). Longitudinal comparison of two severities of unilateral cervical spinal cord injury using magnetic resonance imaging in rats. J. Neurotrauma 25, 1-18
17. Sparrey, C.J., Salegio, E.A., Camisa, W., Tam, H., Beattie, M.S., Bresnahan, J.C. (2015). Mechanical design and analysis of a unilateral servical spinal cord contusion injury model in nonhuman primates. J. Neurotrauma (in press
18. Nielson, J.L., Haefeli, J., Salegio, E.A., Liu, A.W., Guandique, C.F., Stuck, E.D., Hawbecker, S., Moseanko, R., Strand, S.C., Zdunowski, S., Brock, J.H., Roy, R.R., Rosenzweig, E.S., Nout, Y.S., Courtine, G., Havton, L.A., Steward, O., Edgerton, V.R., Tuszynski, M.H., Beattie, M.S., Bresnahan, J.C., and Ferguson, A.R. (2014). Leveraging biomedical informatics for assessing plasticity and repair in primate spinal cord injury. Brain Res. 1619, 124-138
19. Rosenzweig, E.S., Brock, J.H., Culbertson, M.D., Lu., P., Moseanko, R., Edgerton, V.R., Havton, L.A., and Tuszynski, M.H. (2009). Extensive spinal decussation and bilateral termination of cervical corticospinal projections in rhesus monkeys. J. Comp. Neurol. 513, 151-163
20. Bohannon, R.W., and Smith, M.B. (1987). Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys. Ther. 67, 206-207
21. Salegio, E.A., Kells, A.P., Richardson, R.M., Hadaczek, P., Forsayeth, J., Bringas, J., Sardi, S.P., Passini, M.A., Shihabuddin, L.S., Cheng, S.H., Fiandaca, M.S., and Bankiewicz, K.S. (2010). Magnetic resonance imaging-guided delivery of adeno-Associated virus type 2 to the primate brain for the treatment of lysosomal storage disorders. Hum. Gene Ther. 21, 1093-1103
22. Bresnahan, J.C., Beattie, M.S., Todd, F.D. 3rd, and Noyes, D.H. (1987) A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device. Exp. Neurol. 95, 548-570
23. Irvine, K.A., Ferguson, A.R., Mitchell, K.D., Beattie, S.B., Lin, A., Stuck, E.D., Huie, J.R., Nielson, J.L., Talbott, J.F., Inoue, T., Beattie, M.S., and Bresnahan, J.C. (2014). The Irvine, Beatties, and Bresnahan (IBB) forelimb recovery scale: an assessment of reliability and validity. Front. Neurol. 5, 116
24. Bresnahan, J.C., King, J.S., Martin, G.F., and Yashon, D. (1976) A neuroanatomical analysis of spinal cord injury in the rhesus monkey (Macaca mulatta). J. Neurol. Sci. 28, 521-542
25. Lindsey, A.E., LoVerso, R.L., Tovar, C.A., Hill, C.E., Beattie, M.S., and Bresnahan, J.C. (2000). An analysis of changes in sensory thresholds to mild tactile and cold stimuli after experimental spinal cord injury in the rat. Neurorehabil. Neural Repair 14, 287-300
26. Bresnahan, J.C., Behrmann, D.L., and Beattie, M.S. (1993). Anatomical and behavioral outcome after spinal cord contusion injury produced by a displacement controlled impact device. Restor. Neurol. Neurosci. 5, 76
27. Allen, A.R. (1911). Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column: a preliminary report. JAMA. 57, 878-880
28. Bresnahan, J.C. (1978). An electron-microscopic analysis of axonal alterations following blunt contusion of the spinal cord of the rhesus monkey (Macaca mulatta). J. Neurol. Sci. 37, 59-82
29. Young, W., DeCrescito, V., Flamm, E.S., Blight, A.R., and Gruner, J.A. (1988). Pharmacological therapy of acute spinal cord injury: studies of high dose methylprednisolone and naloxone. Clin. Neurosurg. 34, 675-697
30. Young, W., and Flamm, E.S. (1982). Effect of high-dose corticosteroid therapy on blood flow, evoked potentials, and extracellular calcium in experimental spinal injury. J. Neurosurg. 57, 667-673
31. Hall, E.D., and Braughler, J.M. (1982). Effects of intravenous methylprednisolone on spinal cord lipid peroxidation and Na+ + K+)-ATPase activity. Dose-response analysis during 1st hour after contusion injury in the cat. J. Neurosurg. 57, 247-253
32. Means, E.D., Anderson, D.K., Waters, T.R., and Kalaf, L. (1981). Effect of methylprednisolone in compression trauma to the feline spinal cord. J. Neurosurg. 55, 200-208
33. Basso, D.M., Beattie, M.S., Bresnahan, J.C., Anderson, D.K., Faden, A.I., Gruner, J.A., Holford, T.R., Hsu, C.Y., Noble, L.J., Nockels, R., Perot, P.L., Salzman, S.K., and Young, W. (1996). MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J. Neurotrauma 13, 343-359
34. Young, W. (2009). MASCIS spinal cord contusion model. In: Animal Models of Acute Neurological Injuries. J. Chen, X.M. Xu, and Z. Xu (eds). Humana Press: New York, pps. 411-421
35. Noyes, D.H. (1987). Electromechanical impactor for producing experimental spinal cord injury in animals. Med. Biol. Eng. Comput. 25, 335-340
36. Somerson, S.K., and Stokes, B.T. (1987). Functional analysis of an electromechanical spinal cord injury device. Exp. Neurol. 96, 82-96
37. Behrmann, D.L., Bresnahan, J.C., Beattie, M.S., and Shah, B.R. (1992). Spinal cord injury produced by consistent mechanical displacement of the cord in rats: behavioral and histologic analysis. J. Neurotrauma 9, 197-217
38. Scheff, S.W., Rabchevsky, A.G., Fugaccia, I., Main, J.A., and Lumpp, J.E., Jr. (2003). Experimentalmodeling of spinal cord injury: characterization of a force-defined injury device. J. Neurotrauma 20, 179-193
39. Choo, A.M., Liu, J., Lam, C.K., Dvorak, M., Tetzlaff, W., and Oxland, T.R. (2007). Contusion, dislocation, and distraction: primary hemorrhage and membrane permeability in distinct mechanisms of spinal cord injury. J. Neurosurg. Spine 6, 255-266
40. Choo, A.M., Liu, J., Liu, Z., .Dvorak, M., Tetzlaff, W., and Oxland, T.R. (2009). Modeling spinal cord contusion, dislocation, and distraction: characterization of vertebral clamps, injury severities, and node of Ranvier deformations. J. Neurosci. Methods 181, 6-17
41. Shetye, S.S., Troyer, K.L., Streijger, F., Lee, J.H., Kwon, B.K., Cripton, P.A., and Puttlitz, C.M. (2014). Nonlinear viscoelastic characterization of the porcine spinal cord. Acta. Biomater. 10, 792-797
42. Stokes, B.T., Noyes, D.H., and Behrmann, D.L. (1992). An electromechanical spinal injury technique with dynamic sensitivity. J. Neurotrauma 9, 187-195
43. Behrmann, D.L., Bresnahan, J.C., and Beattie, M.S. (1993) A comparison of YM-14673, U-50488H, and nalmefene after spinal cord injury in the rat. Exp. Neurol. 119, 258-267
44. Behrmann, D.L., Bresnahan, J.C., and Beattie, M.S. (1994). Modeling of acute spinal cord injury in the rat: neuroprotection and enhanced recovery with methylprednisolone, U-74006F and YM-14673. Exp. Neurol. 126, 61-75
45. Romanowski, K., Nout, Y.S., Beattie, M.S., Bresnahan, J.C., and Sparrey, C.J. (2011). Interspecies Variation in Spinal Cord and Column Morphology and Its Affect on Cord Compression Mechanics. Society for Neuroscience: Washington, D.C
46. Sparrey, C.J., Choo, A.M., Liu, J., Tetzlaff, W., and Oxland, T.R. (2008). The distribution of tissue damage in the spinal cord is influenced by the contusion velocity. Spine 33, E812-E819
47. Lam, C.J., Assinck, P., Liu, J., Tetzlaff, W., and Oxland, T.R. (2014). Impact depth and the interaction with impact speed affect the severity of contusion spinal cord injury in rats. J. Neurotrauma 31, 1985-1997
48. Gledhill, R.F., Harrison, B.M., and McDonald, W.I. (1973). Demyelination and remyelination after acute spinal cord compression. Exp. Neurol. 38, 472-487
49. Lee, J.H., Jones, C.F., Okon, E.B., Anderson, L., Tigchelaar, S., Kooner, P., Godbey, T., Chua, B., Gray, G., Hildebrandt, R., Cripton, P., Tetzlaff, W., and Kwon, B.K. (2013) A novel porcine model of traumatic thoracic spinal cord injury. J. Neurotrauma 30, 142-159
50. Jones, C.F., Kwon, B.K., and Cripton, P.A. (2012). Mechanical indicators of injury severity are decreased with increased thecal sac dimension in a bench-top model of contusion type spinal cord injury. J. Biomech. 45, 1003-1010
51. Nishimura, Y., Morichika, Y., and Isa, T. (2009) A subcortical oscillatory network contributes to recovery of hand dexterity after spinal cord injury. Brain 132, 709-721
52. Nishimura, Y., Onoe, H., Morichika, Y., Perfiliev, S., Tsukada, H., and Isa, T. (2007). Time-dependent central compensatory mechanisms of finger dexterity after spinal cord injury. Science 318, 1150-1155
53. Alstermark, B., and Isa, T. (2012). Circuits for skilled reaching and grasping. Annu. Rev. Neurosci. 35, 559-578
54. Fouad, K., Klusman, I., and Schwab, M.E. (2004). Regenerating corticospinal fibers in the Marmoset (Callitrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur. J. Neurosci. 20, 2479-2482
55. Freund, P., Schmidlin, E., Wannier, T., Bloch, J., Mir, A., Schwab, M.E., and Rouiller, E.M. (2006). Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 12, 790-792
56. Freund, P., Wannier, T., Schmidlin, E., Bloch, J., Mir, A., Schwab, M.E., and Rouiller, E.M. (2007). Anti-Nogo-A antibody treatment enhances sprouting of corticospinal axons rostral to a unilateral cervical spinal cord lesion in adult macaque monkey. J. Comp. Neurol. 502, 644-659
57. Inoue, T., Lin, A., Ma, X., McKenna, S.L., Creasey, G.H., Manley, G.T., Ferguson, A.R., Bresnahan, J.C., and Beattie, M.S. (2013). Combined SCI and TBI: recovery of forelimb function after unilateral cervical spinal cord injury (SCI) is retarded by contralateral traumatic brain injury (TBI), and ipsilateral TBI balances the effects of SCI on paw placement. Exp. Neurol. 248, 136-147
58. Ringner, M. (2008). What is principal component analysis?. Nat. Biotechnol. 26, 303-304
59. Mahmood, N.S., Kadavigere, R., Avinash, K.R., and Rao, V.R. (2008). Magnetic resonance imaging in acute cervical spinal cord injury: a correlative study on spinal cord changes and 1 month motor recovery. Spinal Cord 46, 791-797
60. Ramon, S., Dominguez, R., Ramirez, L., Paraira, M., Olona, M., Castello, T., and Garcia Fernandez, L. (1997). Clinical and magnetic resonance imaging correlation in acute spinal cord injury. Spinal Cord 35, 664-673
61. Lammertse, D., Dungan, D., Dreisbach, J., Falci, S., Flanders, A., Marino, R., and Schwartz, E. National Institute on Disability and Rehabilitation. (2007). Neuroimaging in traumatic spinal cord injury: an evidence-based review for clinical practice and research. J. Spinal Cord Med. 30, 205-214
62. Denny-Brown, D., Kirk, E.J., and Yanagisawa, N. (1973). The tract of Lissauer in relation to sensory transmission in the dorsal horn of spinal cord in the macaque monkey. J. Comp. Neurol. 151, 175-200
63. Brown-Sequard, C.E. (1849). De la transmission des impressions sensitives par la moelle epiniere. C. R. Soc. Biol. 1, 192-194
64. Kalsi-Ryan, S., Beaton, D., Curt, A., Popovic, M.R., Verrier, M.C., and Fehlings, M.G. (2014). Outcome of the upper limb in cervical spinal cord injury: profiles of recovery and insights for clinical studies. J. Spinal Cord Med. 37, 503-510
65. University of Alabama. (2014). National Spinal Cord Injury Statistical Center, Facts and Figures at a Glance. Available at: www.nscisc.uab.edu. Accessed November 21, 2015
66. Lu, P., Wang, Y., Graham, L., McHale, K., Gao, M., Wu, D., Brock, J., Blesch, A., Rosenzweig, E.S., Havton, L.A., Zheng, B., Conner, J.M., Marsala, M., and Tuszynski, M.H. (2012). Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 150, 1264-1273