Cerebrospinal fluid inflammatory cytokines and biomarkers of injury severity in acute human spinal cord injury

Journal of Neurotrauma

Volumn 27, Issue 4, 2010, Pages 669-682

  Kwon, Brian K ^a   Stammers, Anthea M T ^a   Belanger, Lise M ^b   Bernardo, Arlene ^b   Chan, Donna ^b   Bishop, Carole M ^b   Slobogean, Gerard P ^a   Zhang, Hongbin ^b   Umedaly, Hamed ^a   Giffin, Mitch ^a   Street, John ^a   Boyd, Michael C ^a   Paquette, Scott J ^a   Fisher, Charles G ^a   Dvorak, Marcel F ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b VANCOUVER GENERAL HOSPITAL   (Canada)

Author keywords

Biomarkers; Cerebrospinal fluid; Clinical trial; Inflammation; Traumatic spinal cord injury

Indexed keywords

BIOLOGICAL MARKER; CYTOKINE; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN S100B; TAU PROTEIN;

ACCURACY; ADULT; ARTICLE; CEREBROSPINAL FLUID; CEREBROSPINAL FLUID ANALYSIS; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CONVALESCENCE; DISEASE MARKER; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; INJURY SEVERITY; MALE; MOTOR PERFORMANCE; NEUROPATHIC PAIN; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PREDICTOR VARIABLE; PROTEIN EXPRESSION; RATING SCALE; SPINAL CORD INJURY; VALIDATION PROCESS;

ADULT; BIOLOGICAL MARKERS; CHEMOKINE CCL2; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-6; INTERLEUKIN-8; MALE; MIDDLE AGED; MYELITIS; NERVE GROWTH FACTORS; PREDICTIVE VALUE OF TESTS; PROGNOSIS; PROSPECTIVE STUDIES; RECOVERY OF FUNCTION; S100 PROTEINS; SPINAL CORD; SPINAL CORD INJURIES; TAU PROTEINS; TRAUMA SEVERITY INDICES; YOUNG ADULT;

EID: 77951287743     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2009.1080     Document Type: Article

References (64)

1. Abdellatif, A.A., Pelt, J.L., Benton, R.L., Howard, R.M., Tsoulfas, P., Ping, P., Xu, X.M., and Whittemore, S.R. (2006). Gene delivery to the spinal cord: Comparison between lentiviral, adenoviral, and retroviral vector delivery systems. J. Neurosci. Res. 84, 553-567. (Pubitemid 44196696)
2. American Spinal Injury Association/International Medical Society of Paraplegia. (2000). International standards for neurological and functional classification of spinal cord injury patients.
3. Austin, P.C., and Tu, J.V. (2004). Bootstrap methods for developing predictive models. Am. Stat. 58, 131-137.
4. Bennett, M.I., Attal, N., Backonja, M.M., Baron, R., Bouhassira, D., Freynhagen, R., Scholz, J., Tolle, T.R., Wittchen, H.U., and Jensen, T.S. (2007). Using screening tools to identify neuropathic pain. Pain 127, 199-203. (Pubitemid 46084881)
5. Bouhy, D., Malgrange, B., Multon, S., Poirrier, A.L., Scholtes, F., Schoenen, J., and Franzen, R. (2006). Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via an increased BDNF expression by endogenous macrophages. FASEB J. 20, 1239-1241. (Pubitemid 44943884)
6. Burchiel, K.J., and Hsu, F.P. (2001). Pain and spasticity after spinal cord injury: Mechanisms and treatment. Spine 26, S146-S160.
7. Burns, A.S., and Ditunno, J.F. (2001). Establishing prognosis and maximizing functional outcomes after spinal cord injury: A review of current and future directions in rehabilitation management. Spine 26, S137-S145.
8. Burns, A.S., Lee, B.S., Ditunno, J.F., Jr., and Tessler, A. (2003). Patient selection for clinical trials: The reliability of the early spinal cord injury examination. J. Neurotrauma 20, 477-482. (Pubitemid 36617950)
9. Chatfield, D.A., Zemlan, F.P., Day, D.J., and Menon, D.K. (2002). Discordant temporal patterns of S100beta and cleaved tau protein elevation after head injury: A pilot study. Br. J. Neurosurg. 16, 471-476.
10. Demjen, D., Klussmann, S., Kleber, S., Zuliani, C., Stieltjes, B., Metzger, C., Hirt, U.A., Walczak, H., Falk, W., Essig, M., Edler, L., Krammer, P.H., and Martin-Villalba, A. (2004). Neutralization of CD95 ligand promotes regeneration and functional recovery after spinal cord injury. Nat. Med. 10, 389-395. (Pubitemid 38508517)
11. Detloff, M.R., Fisher, L.C., McGaughy, V., Longbrake, E.E., Popovich, P.G., and Basso, D.M. (2008). Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp. Neurol. 212, 337-347.
12. Ditor, D.S., Bao, F., Chen, Y., Dekaban, G.A., and Weaver, L.C. (2006). A therapeutic time window for anti-CD 11d monoclonal antibody treatment yielding reduced secondary tissue damage and enhanced behavioral recovery following severe spinal cord injury. J. Neurosurg. Spine 5, 343-352. (Pubitemid 47325374)
13. Fawcett, J.W., Curt, A., Steeves, J.D., Coleman, W.P., Tuszynski, M.H., Lammertse, D., Bartlett, P.F., Blight, A.R., Dietz, V., Ditunno, J., Dobkin, B.H., Havton, L.A., Ellaway, P.H., Fehlings, M.G., Privat, A., Grossman, R., Guest, J.D., Kleitman, N., Nakamura, M., Gaviria, M., and Short, D. (2007). Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: Spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 45, 190-205. (Pubitemid 46340848)
14. Fehlings, M.G., and Baptiste, D.C. (2005). Current status of clinical trials for acute spinal cord injury. Injury 36 Suppl 2, B113-B122.
15. Fleming, J.C., Norenberg, M.D., Ramsay, D.A., Dekaban, G.A., Marcillo, A.E., Saenz, A.D., Pasquale-Styles, M., Dietrich, W.D., and Weaver, L.C. (2006). The cellular inflammatory response in human spinal cords after injury. Brain 129, 3249-3269. (Pubitemid 44871440)
16. 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. (Pubitemid 44050068)
17. Geisler, F.H., Coleman, W.P., Grieco, G., and Poonian, D. (2001a). Measurements and recovery patterns in a multicenter study of acute spinal cord injury. Spine 26, S68-S86. (Pubitemid 34019782)
18. Geisler, F.H., Coleman, W.P., Grieco, G., and Poonian, D. (2001b). The Sygen multicenter acute spinal cord injury study. Spine 26, S87-S98. (Pubitemid 34019783)
19. Geisler, F.H., Dorsey, F.C., and Coleman, W.P. (1991). Recovery of motor function after spinal-cord injury - A randomized, placebo-controlled trial with GM-1 ganglioside. N. Engl. J. Med. 324, 1829-1838.
20. Genovese, T., Mazzon, E., Crisafulli, C., Di Paola, R., Muia, C., Bramanti, P., and Cuzzocrea, S. (2006). Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther. 316, 1006-1016. (Pubitemid 43345272)
21. Ghirnikar, R.S., Lee, Y.L., and Eng, L.F. (2000). Chemokine antagonist infusion attenuates cellular infiltration following spinal cord contusion injury in rat. J. Neurosci. Res. 59, 63-73.
22. Ghirnikar, R.S., Lee, Y.L., and Eng, L.F. (2001). Chemokine antagonist infusion promotes axonal sparing after spinal cord contusion injury in rat. J. Neurosci. Res. 64, 582-589.
23. Glaser, J., Gonzalez, R., Perreau, V.M., Cotman, C.W., and Keirstead, H.S. (2004). Neutralization of the chemokine CXCL10 enhances tissue sparing and angiogenesis following spinal cord injury. J. Neurosci. Res. 77, 701-708. (Pubitemid 39194611)
24. Glaser, J., Gonzalez, R., Sadr, E., and Keirstead, H.S. (2006). Neutralization of the chemokine CXCL10 reduces apoptosis and increases axon sprouting after spinal cord injury. J. Neurosci. Res. 84, 724-734. (Pubitemid 44366674)
25. Gonzalez, R., Glaser, J., Liu, M.T., Lane, T.E., and Keirstead, H.S. (2003). Reducing inflammation decreases secondary degeneration and functional deficit after spinal cord injury. Exp. Neurol. 184, 456-463. (Pubitemid 37444053)
26. Gonzalez, R., Hickey, M.J., Espinosa, J.M., Nistor, G., Lane, T.E., and Keirstead, H.S. (2007). Therapeutic neutralization of CXCL10 decreases secondary degeneration and functional deficit after spinal cord injury in mice. Regen. Med. 2, 771-783. (Pubitemid 47554831)
27. Gorio, A., Madaschi, L., Di Stefano, B., Carelli, S., Di Giulio, A.M., De Biasi, S., Coleman, T., Cerami, A., and Brines, M. (2005). Methylprednisolone neutralizes the beneficial effects of erythropoietin in experimental spinal cord injury. Proc. Natl. Acad. Sci. USA 102, 16379-16384. (Pubitemid 41688922)
28. Guez, M., Hildingsson, C., Rosengren, L., Karlsson, K., and Toolanen, G. (2003). Nervous tissue damage markers in cerebrospinal fluid after cervical spine injuries and whiplash trauma. J. Neurotrauma 20, 853-858. (Pubitemid 37159067)
29. Harrington, J.F., Messier, A.A., Levine, A., Szmydynger-Chodobska, J., and Chodobski, A. (2005). Shedding of tumor necrosis factor type 1 receptor after experimental spinal cord injury. J. Neurotrauma 22, 919-928. (Pubitemid 41153876)
30. Jones, T.B., McDaniel, E.E., and Popovich, P.G. (2005). Inflammatory-mediated injury and repair in the traumatically injured spinal cord. Curr. Pharm. Des. 11, 1223-1236. (Pubitemid 40458268)
31. Kaplin, A.I., Deshpande, D.M., Scott, E., Krishnan, C., Carmen, J.S., Shats, I., Martinez, T., Drummond, J., Dike, S., Pletnikov, M., Keswani, S.C., Moran, T.H., Pardo, C.A., Calabresi, P.A., and Kerr, D.A. (2005). IL-6 induces regionally selective spinal cord injury in patients with the neuroinflammatory disorder transverse myelitis. J. Clin. Invest. 115, 2731-2741. (Pubitemid 41434400)
32. Kwon, B.K., Curt, A., Belanger, L.M., Bernardo, A., Chan, D., Markez, J.A., Gorelik, S., Slobogean, G.P., Umedaly, H., Giffin, M., Nikolakis, M.A., Street, J., Boyd, M.C., Paquette, S., Fisher, C.G., and Dvorak, M.F. (2009). Intrathecal pressure monitoring and cerebrospinal fluid drainage in acute spinal cord injury: A prospective randomized trial. J. Neurosurg. Spine 10, 181-193.
33. Lacroix, S., Chang, L., Rose-John, S., and Tuszynski, M.H. (2002). Delivery of hyper-interleukin-6 to the injured spinal cord increases neutrophil and macrophage infiltration and inhibits axonal growth. J. Comp. Neurol. 454, 213-228. (Pubitemid 35423832)
34. Lammertse, D., Tuszynski, M.H., Steeves, J.D., Curt, A., Fawcett, J.W., Rask, C., Ditunno, J.F., Fehlings, M.G., Guest, J.D., Ellaway, P.H., Kleitman, N., Blight, A.R., Dobkin, B.H., Grossman, R., Katoh, H., Privat, A., and Kalichman, M. (2007). Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: Clinical trial design. Spinal Cord 45, 232-242. (Pubitemid 46340851)
35. Lammertse, D.P. (2004). Update on pharmaceutical trials in acute spinal cord injury. J. Spinal Cord Med. 27, 319-325. (Pubitemid 44132771)
36. Marchand, F., Tsantoulas, C., Singh, D., Grist, J., Clark, A.K., Bradbury, E.J., and McMahon, S.B. (2009). Effects of Etanercept and Minocycline in a rat model of spinal cord injury. Eur. J. Pain 13, 673-681.
37. Marino, R.J., Ditunno, J.F., Jr., Donovan, W.H., and Maynard, F., Jr. (1999). Neurologic recovery after traumatic spinal cord injury: Data from the Model Spinal Cord Injury Systems. Arch. Phys. Med. Rehabil. 80, 1391-1396. (Pubitemid 29526635)
38. Moalem, G., and Tracey, D.J. (2006). Immune and inflammatory mechanisms in neuropathic pain. Brain Res. Brain Res. Rev. 51, 240-264. (Pubitemid 43902971)
39. Nakamura, M., Houghtling, R.A., MacArthur, L., Bayer, B.M., and Bregman, B.S. (2003). Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp. Neurol. 184, 313-325. (Pubitemid 37444041)
40. Nakamura, M., Okada, S., Toyama, Y., and Okano, H. (2005). Role of IL-6 in spinal cord injury in a mouse model. Clin. Rev. Allergy Immunol. 28, 197-204. (Pubitemid 41208909)
41. Nishimoto, N., Miyasaka, N., Yamamoto, K., Kawai, S., Takeuchi, T., and Azuma, J. (2009). Long-term safety and efficacy of tocilizumab, an anti-interleukin-6 receptor monoclonal antibody, in monotherapy, in patients with rheumatoid arthritis (the STREAM study): Evidence of safety and efficacy in a 5-year extension study. Ann. Rheum. Dis. 68, 1580-1584.
42. O'Collins, V.E., Macleod, M.R., Donnan, G.A., Horky, L.L., van der Worp, B.H., and Howells, D.W. (2006). 1,026 experimental treatments in acute stroke. Ann. Neurol. 59, 467-477.
43. Okada, S., Nakamura, M., Mikami, Y., Shimazaki, T., Mihara, M., Ohsugi, Y., Iwamoto, Y., Yoshizaki, K., Kishimoto, T., Toyama, Y., and Okano, H. (2004). Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J. Neurosci. Res. 76, 265-276. (Pubitemid 38451214)
44. Ost, M., Nylen, K., Csajbok, L., Ohrfelt, A.O., Tullberg, M., Wikkelso, C., Nellgard, P., Rosengren, L., Blennow, K., and Nellgard, B. (2006). Initial CSF total tau correlates with 1-year outcome in patients with traumatic brain injury. Neurology 67, 1600-1604. (Pubitemid 44747930)
45. Ousman, S.S., and David, S. (2001). MIP-1alpha, MCP-1, GMCSF, and TNF-alpha control the immune cell response that mediates rapid phagocytosis of myelin from the adult mouse spinal cord. J. Neurosci. 21, 4649-4656. (Pubitemid 32565623)
46. Pearse, D.D., Marcillo, A.E., Oudega, M., Lynch, M.P., Wood, P.M., and Bunge, M.B. (2004). Transplantation of Schwann cells and olfactory ensheathing glia after spinal cord injury: Does pretreatment with methylprednisolone and interleukin-10 enhance recovery? J. Neurotrauma 21, 1223-1239. (Pubitemid 39280849)
47. Peng, X.M., Zhou, Z.G., Glorioso, J.C., Fink, D.J., and Mata, M. (2006). Tumor necrosis factor-alpha contributes to below-level neuropathic pain after spinal cord injury. Ann. Neurol. 59, 843-851. (Pubitemid 43673162)
48. Pouw, M.H., Hosman, A.J., van Middendorp, J.J., Verbeek, M.M., Vos, P.E., and van de Meent, H. (2009). Biomarkers in spinal cord injury. Spinal Cord 47, 519-525.
49. Ramer, M.S., Harper, G.P., and Bradbury, E.J. (2000). Progress in spinal cord research - A refined strategy for the International Spinal Research Trust. Spinal Cord 38, 449-472.
50. Sawatzky, B., Bishop, C.M., and Miller, W.C. (2008). Classification and measurement of pain in the spinal cord-injured population. Spinal Cord 46, 2-10.
51. Siddall, P.J., and Middleton, J.W. (2006). A proposed algorithm for the management of pain following spinal cord injury. Spinal Cord 44, 67-77. (Pubitemid 43190349)
52. Siddall, P.J., McClelland, J.M., Rutkowski, S.B., and Cousins, M.J. (2003). A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain 103, 249-257.
53. Siddall, P.J., Taylor, D.A., McClelland, J.M., Rutkowski, S.B., and Cousins, M.J. (1999). Pain report and the relationship of pain to physical factors in the first 6 months following spinal cord injury. Pain 81, 187-197.
54. Sommer, C. (1999). [Animal studies on neuropathic pain: The role of cytokines and cytokine receptors in pathogenesis and therapy]. Schmerz 13, 315-323. (Pubitemid 29500855)
55. Tator, C.H. (2006). Review of treatment trials in human spinal cord injury: Issues, difficulties, and recommendations. Neurosurgery 59, 957-982. (Pubitemid 44852056)
56. Trivedi, A., Olivas, A.D., and Noble-Haeusslein, L.J. (2006). Inflammation and spinal cord injury: Infiltrating leukocytes as determinants of injury and repair processes. Clin. Neurosci. Res. 6, 283-292. (Pubitemid 44849178)
57. Wang, C.X., Olschowka, J.A., and Wrathall, J.R. (1997). Increase of interleukin-1beta mRNA and protein in the spinal cord following experimental traumatic injury in the rat. Brain Res. 759, 190-196. (Pubitemid 27286694)
58. Waters, R.L., Adkins, R.H., Yakura, J.S., and Sie, I. (1993). Motor and sensory recovery following complete tetraplegia. Arch. Phys. Med. Rehabil. 74, 242-247. (Pubitemid 23083796)
59. Waters, R.L., Adkins, R.H., Yakura, J.S., and Sie, I. (1994). Motor and sensory recovery following incomplete tetraplegia. Arch. Phys. Med. Rehabil. 75, 306-311. (Pubitemid 24099564)
60. Yamasaki, Y., Matsuo, Y., Zagorski, J., Matsuura, N., Onodera, H., Itoyama, Y., and Kogure, K. (1997). New therapeutic possibility of blocking cytokine-induced neutrophil chemoattractant on transient ischemic brain damage in rats. Brain Res. 759, 103-111. (Pubitemid 27286349)
61. Yan, J., Welsh, A.M., Bora, S.H., Snyder, E.Y., and Koliatsos, V.E. (2004). Differentiation and tropic/trophic effects of exogenous neural precursors in the adult spinal cord. J. Comp. Neurol. 480, 101-114. (Pubitemid 39453140)
62. Yan, P., Liu, N., Kim, G.M., Xu, J., Xu, J., Li, Q., Hsu, C.Y., and Xu, X.M. (2003). Expression of the type 1 and type 2 receptors for tumor necrosis factor after traumatic spinal cord injury in adult rats. Exp. Neurol. 183, 286-297. (Pubitemid 37205071)
63. Yang, L., Blumbergs, P.C., Jones, N.R., Manavis, J., Sarvestani, G.T., and Ghabriel, M.N. (2004). Early expression and cellular localization of proinflammatory cytokines interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in human traumatic spinal cord injury. Spine 29, 966-971. (Pubitemid 38580232)
64. Yang, L., Jones, N.R., Blumbergs, P.C., Van Den, H.C., Moore, E.J., Manavis, J., Sarvestani, G.T., and Ghabriel, M.N. (2005). Severity-dependent expression of pro-inflammatory cytokines in traumatic spinal cord injury in the rat. J. Clin. Neurosci. 12, 276-284. (Pubitemid 40585726)