Derivation of Multivariate Syndromic Outcome Metrics for Consistent Testing across Multiple Models of Cervical Spinal Cord Injury in Rats

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Ferguson, Adam R ^a   Irvine, Karen Amanda ^b   Gensel, John C ^c   Nielson, Jessica L ^a   Lin, Amity ^a   Ly, Johnathan ^a   Segal, Mark R ^a   Ratan, Rajiv R ^d   Bresnahan, Jacqueline C ^a   Beattie, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD INJURY; CONSTRUCT VALIDITY; CONTROLLED STUDY; DISEASE MODEL; DISEASE SEVERITY; EXTERNAL VALIDITY; FACE VALIDITY; FEMALE; FUNCTIONAL ASSESSMENT; GAIT; GRAY MATTER; HISTOPATHOLOGY; INFORMATION PROCESSING; INJURY SEVERITY; LOCOMOTION; NEUROBIOLOGY; NONHUMAN; OPEN FIELD TEST; OUTCOME ASSESSMENT; PRINCIPAL COMPONENT ANALYSIS; RAT; RELIABILITY; SENSITIVITY ANALYSIS; VALIDATION PROCESS; WHITE MATTER;

ANIMALS; BEHAVIOR, ANIMAL; CERVICAL VERTEBRAE; CONTUSIONS; DISEASE MODELS, ANIMAL; FEMALE; LOCOMOTION; MULTIVARIATE ANALYSIS; PRINCIPAL COMPONENT ANALYSIS; RATS; RATS, LONG-EVANS; RECOVERY OF FUNCTION; REPRODUCIBILITY OF RESULTS; SEVERITY OF ILLNESS INDEX; SPINAL CORD INJURIES; SYNDROME;

RATTUS;

EID: 84875409052     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059712     Document Type: Article

References (64)

1. Chan AW, Hrobjartsson A, Haahr MT, Gotzsche PC, Altman DG, (2004) Empirical evidence for selective reporting of outcomes in randomized trials: comparison of protocols to published articles. Jama 291: 2457-2465.
2. Evans JA, Foster JG, (2011) Metaknowledge. Science 331: 721-725.
3. Pinzon A, Marcillo A, Pabon D, Bramlett HM, Bunge MB, et al. (2008) A re-assessment of erythropoietin as a neuroprotective agent following rat spinal cord compression or contusion injury. Exp Neurol 213: 129-136.
4. Pinzon A, Marcillo A, Quintana A, Stamler S, Bunge MB, et al. (2008) A re-assessment of minocycline as a neuroprotective agent in a rat spinal cord contusion model. Brain Res 1243: 146-151.
5. Sena E, van der Worp HB, Howells D, Macleod M, (2007) How can we improve the pre-clinical development of drugs for stroke? Trends Neurosci 30: 433-439.
6. Sharp K, Flanagan L, Yee KM, Steward O (2010) A re-assessment of a combinatorial treatment involving Schwann cell transplants and elevation of cyclic AMP on recovery of motor function following thoracic spinal cord injury in rats. Exp Neurol.
7. Steward O, Sharp K, Selvan G, Hadden A, Hofstadter M, et al. (2006) A re-assessment of the consequences of delayed transplantation of olfactory lamina propria following complete spinal cord transection in rats. Exp Neurol 198: 483-499.
8. Steward O, Sharp K, Yee KM, Hofstadter M, (2008) A re-assessment of the effects of a Nogo-66 receptor antagonist on regenerative growth of axons and locomotor recovery after spinal cord injury in mice. Exp Neurol 209: 446-468.
9. McIntosh TK, Noble L, Andrews B, Faden AI, (1987) Traumatic brain injury in the rat: characterization of a midline fluid-percussion model. Cent Nerv Syst Trauma 4: 119-134.
10. Andersen CS, Andersen AB, Finger S, (1991) Neurological correlates of unilateral and bilateral "strokes" of the middle cerebral artery in the rat. Physiol Behav 50: 263-269.
11. Basso DM, Beattie MS, Bresnahan JC, (1995) A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12: 1-21.
12. Gale K, Kerasidis H, Wrathall JR, (1985) Spinal cord contusion in the rat: behavioral analysis of functional neurologic impairment. Exp Neurol 88: 123-134.
13. Grau JW, Washburn SN, Hook MA, Ferguson AR, Crown ED, et al. (2004) Uncontrollable stimulation undermines recovery after spinal cord injury. J Neurotrauma 21: 1795-1817.
14. Courtine G, Gerasimenko Y, van den Brand R, Yew A, Musienko P, et al. (2009) Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12: 1333-1342.
15. van den Brand R, Heutschi J, Barraud Q, DiGiovanna J, Bartholdi K, et al. (2012) Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 336: 1182-1185.
16. Dominici N, Keller U, Vallery H, Friedli L, van den Brand R, et al. (2012) Versatile robotic interface to evaluate, enable and train locomotion and balance after neuromotor disorders. Nat Med 18: 1142-1147.
17. Rosenzweig ES, Courtine G, Jindrich DL, Brock JH, Ferguson AR, et al. (2010) Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 13: 1505-1510.
18. Chretien JP, Burkom HS, Sedyaningsih ER, Larasati RP, Lescano AG, et al. (2008) Syndromic surveillance: adapting innovations to developing settings. PLoS Med 5: e72.
19. Ferguson AR, Stuck ED, Nielson JL, (2011) Syndromics: A Bioinformatics Approach for Neurotrauma Research. Transl Stroke Res 2: 438-454.
20. Ferguson AR, Hook MA, Garcia G, Bresnahan JC, Beattie MS, et al. (2004) A simple post hoc transformation that improves the metric properties of the BBB scale for rats with moderate to severe spinal cord injury. J Neurotrauma 21: 1601-1613.
21. Young W, (2002) Spinal cord contusion models. Prog Brain Res 137: 231-255.
22. Gensel JC, Tovar CA, Hamers FP, Deibert RJ, Beattie MS, et al. (2006) Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J Neurotrauma 23: 36-54.
23. Constantini S, Young W, (1994) The effects of methylprednisolone and the ganglioside GM1 on acute spinal cord injury in rats. J Neurosurg 80: 97-111.
24. Gruner JA (1992) A monitored contusion model of spinal cord injury in the rat. J Neurotrauma 9: 123-126; discussion 126-128.
25. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, et al. (1999) Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 19: 4370-4387.
26. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, et al. (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158: 351-365.
27. Hamers FP, Lankhorst AJ, van Laar TJ, Veldhuis WB, Gispen WH, (2001) Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma 18: 187-201.
28. Ferguson AR, Christensen RN, Gensel JC, Miller BA, Sun F, et al. (2008) Cell death after spinal cord injury is exacerbated by rapid TNF alpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. J Neurosci 28: 11391-11400.
29. Pearson K, (1901) On Lines and Planes of Closest Fit to Systems of Points in Space. Philos Mag 2: 559-572.
30. Browne MW, (2001) An overview of analytic rotation in exploratory factor analysis. Multivar Behav Res 36: 111-150.
31. Kaiser HF, (1960) The Application of Electronic-Computers to Factor-Analysis. Educ Psychol Meas 20: 141-151.
32. Cattell RB, (1966) Scree Test for Number of Factors. Multivar Behav Res 1: 245-276.
33. Guadagnoli E, Velicer WF, (1988) Relation of sample size to the stability of component patterns. Psychol Bull 103: 265-275.
34. Cattell RB, Balcar KR, Horn JL, Nesselroade JR (1969) Factor Matching Procedures- an Improvement of S Index- with Tables. Educ Psychol Meas 29: 781-&.
35. Guadagnoli E, Velicer W, (1991) A Comparison of Pattern-Matching Indexes. Multivar Behav Res 26: 323-343.
36. Korth B, Tucker LR, (1976) Procrustes Matching by Congruence Coefficients. Psychometrika 41: 531-535.
37. Witten DM, Tibshirani R, Hastie T, (2009) A penalized matrix decomposition, with applications to sparse principal components and canonical correlation analysis. Biostatistics 10: 515-534.
38. Hook MA, Ferguson AR, Garcia G, Washburn SN, Koehly LM, et al. (2004) Monitoring recovery after injury: procedures for deriving the optimal test window. J Neurotrauma 21: 109-118.
39. Koopmans GC, Deumens R, Honig WM, Hamers FP, Steinbusch HW, et al. (2005) The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J Neurotrauma 22: 214-225.
40. Bresnahan JC, Beattie MS, Todd FD 3rd, Noyes DH (1987) A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device. Exp Neurol 95: 548-570.
41. Noble LJ, Wrathall JR, (1985) Spinal cord contusion in the rat: morphometric analyses of alterations in the spinal cord. Exp Neurol 88: 135-149.
42. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS, (1997) Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3: 73-76.
43. Schwab ME, (2002) Repairing the injured spinal cord. Science 295: 1029-1031.
44. Teng YD, Choi H, Onario RC, Zhu S, Desilets FC, et al. (2004) Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc Natl Acad Sci U S A 101: 3071-3076.
45. Behrmann DL, Bresnahan JC, Beattie MS, (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.
46. McTigue DM, Horner PJ, Stokes BT, Gage FH, (1998) Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci 18: 5354-5365.
47. Rabchevsky AG, Fugaccia I, Sullivan PG, Blades DA, Scheff SW, (2002) Efficacy of methylprednisolone therapy for the injured rat spinal cord. J Neurosci Res 68: 7-18.
48. Gensel JC, Tovar CA, Bresnahan JC, Beattie MS, (2012) Topiramate treatment is neuroprotective and reduces oligodendrocyte loss after cervical spinal cord injury. PLoS One 7: e33519.
49. Scheff SW, Rabchevsky AG, Fugaccia I, Main JA, Lumpp JE Jr, (2003) Experimental modeling of spinal cord injury: characterization of a force-defined injury device. J Neurotrauma 20: 179-193.
50. van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, et al. (2010) Can animal models of disease reliably inform human studies? PLoS Med 7: e1000245.
51. Gorio A, Gokmen N, Erbayraktar S, Yilmaz O, Madaschi L, et al. (2002) Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc Natl Acad Sci U S A 99: 9450-9455.
52. Li S, Strittmatter SM, (2003) Delayed systemic Nogo-66 receptor antagonist promotes recovery from spinal cord injury. J Neurosci 23: 4219-4227.
53. Lu J, Feron F, Mackay-Sim A, Waite PM, (2002) Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 125: 14-21.
54. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, et al. (2004) cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10: 610-616.
55. Wells JE, Hurlbert RJ, Fehlings MG, Yong VW, (2003) Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice. Brain 126: 1628-1637.
56. Popovich PG, Lemeshow S, Gensel JC, Tovar CA, (2012) Independent evaluation of the effects of glibenclamide on reducing progressive hemorrhagic necrosis after cervical spinal cord injury. Exp Neurol 233: 615-622.
57. Simard JM, Tsymbalyuk O, Ivanov A, Ivanova S, Bhatta S, et al. (2007) Endothelial sulfonylurea receptor 1-regulated NC Ca-ATP channels mediate progressive hemorrhagic necrosis following spinal cord injury. J Clin Invest 117: 2105-2113.
58. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH, (2004) Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 24: 6402-6409.
59. Hastie T, Tibshirani R, Friedman J (2009) The Elements of Statistical Learning. New York: Springer.
60. Manley GT, Diaz-Arrastia R, Brophy M, Engel D, Goodman C, et al. (2010) Common data elements for traumatic brain injury: recommendations from the biospecimens and biomarkers working group. Arch Phys Med Rehabil 91: 1667-1672.
61. Biering-Sorensen F, Charlifue S, Devivo MJ, Grinnon ST, Kleitman N, et al. (2012) Using the Spinal Cord Injury Common Data Elements. Topics in spinal cord injury rehabilitation 18: 23-27.
62. Biering-Sorensen F, Charlifue S, Devivo MJ, Grinnon ST, Kleitman N, et al. (2011) Incorporation of the International Spinal Cord Injury Data Set elements into the National Institute of Neurological Disorders and Stroke Common Data Elements. Spinal cord 49: 60-64.
63. Lee JH, Streijger F, Tigchelaar S, Maloon M, Liu J, et al. (2012) A contusive model of unilateral cervical spinal cord injury using the infinite horizon impactor. J Vis Exp.
64. Beattie MS, Ferguson AR, Bresnahan JC, (2010) AMPA-receptor trafficking and injury-induced cell death. Eur J Neurosci 32: 290-297.