Kinematic and dynamic gait compensations in a rat model of lumbar radiculopathy and the effects of tumor necrosis factor-alpha antagonism

Arthritis Research and Therapy

Volumn 13, Issue 4, 2011, Pages

  Allen, Kyle D ^a,b   Shamji, Mohammed F ^a,c   Mata, Brian A ^b   Gabr, Mostafa A ^b   Sinclair, S Michael ^a   Schmitt, Daniel O ^d   Richardson, William J ^b   Setton, Lori A ^a,b  

^a Duke University   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF OTTAWA   (Canada)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA INHIBITOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR TYPE 2; UNCLASSIFIED DRUG; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 2;

ALLODYNIA; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GAIT; GROUND REACTION FORCE; KINEMATICS; LUMBAR RADICULOPATHY; MALE; NOCICEPTION; NONHUMAN; NUCLEUS PULPOSUS; PAW EDEMA; RADICULOPATHY; RAT; SHAM PROCEDURE; WEIGHT BEARING; ADAPTATION; ANIMAL; BACK; BIOMECHANICS; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; HYPERALGESIA; NEUROLOGIC DISEASE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOMECHANICS; DISEASE MODELS, ANIMAL; GAIT; GAIT DISORDERS, NEUROLOGIC; HYPERALGESIA; LUMBOSACRAL REGION; MALE; RADICULOPATHY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; TUMOR NECROSIS FACTOR-ALPHA; WEIGHT-BEARING;

EID: 80052025836     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3451     Document Type: Article

References (60)

1. DeLeo JA, Winkelstein BA. Physiology of chronic spinal pain syndromes: from animal models to biomechanics. Spine (Phila Pa 1976) 2002, 27:2526-2537.
2. Olmarker K, Storkson R, Berge OG. Pathogenesis of sciatic pain: a study of spontaneous behavior in rats exposed to experimental disc herniation. Spine (Phila Pa 1976) 2002, 27:1312-1317.
3. Winkelstein BA, Weinstein JN, DeLeo JA. The role of mechanical deformation in lumbar radiculopathy: an in vivo model. Spine (Phila Pa 1976) 2002, 27:27-33.
4. Olmarker K, Rydevik B. Selective inhibition of tumor necrosis factor-alpha prevents nucleus pulposus-induced thrombus formation, intraneural edema, and reduction of nerve conduction velocity: possible implications for future pharmacologic treatment strategies of sciatica. Spine (Phila Pa 1976) 2001, 26:863-869.
5. Murata Y, Rydevik B, Takahashi K, Larsson K, Olmarker K. Incision of the intervertebral disc induces disintegration and increases permeability of the dorsal root ganglion capsule. Spine (Phila Pa 1976) 2005, 30:1712-1716.
6. Olmarker K, Nutu M, Storkson R. Changes in spontaneous behavior in rats exposed to experimental disc herniation are blocked by selective TNF-alpha inhibition. Spine (Phila Pa 1976) 2003, 28:1635-1641. discussion 1642.
7. Onda A, Murata Y, Rydevik B, Larsson K, Kikuchi S, Olmarker K. Immunoreactivity of brain-derived neurotrophic factor in rat dorsal root ganglion and spinal cord dorsal horn following exposure to herniated nucleus pulposus. Neurosci Lett 2003, 352:49-52. 10.1016/j.neulet.2003.08.025, 14615047.
8. Sasaki N, Kikuchi S, Konno S, Sekiguchi M, Watanabe K. Anti-TNF-alpha antibody reduces pain-behavioral changes induced by epidural application of nucleus pulposus in a rat model depending on the timing of administration. Spine (Phila Pa 1976) 2007, 32:413-416.
9. Shamji MF, Allen KD, So S, Jing L, Adams SB, Schuh R, Huebner J, Kraus VB, Friedman AH, Setton LA, Richardson WJ. Gait abnormalities and inflammatory cytokines in an autologous nucleus pulposus model of radiculopathy. Spine (Phila Pa 1976) 2009, 34:648-654.
10. Suzuki M, Inoue G, Gemba T, Watanabe T, Ito T, Koshi T, Yamauchi K, Yamashita M, Orita S, Eguchi Y, Ochiai N, Kishida S, Takaso M, Aoki Y, Takahashi K, Ohtori S. Nuclear factor-kappa B decoy suppresses nerve injury and improves mechanical allodynia and thermal hyperalgesia in a rat lumbar disc herniation model. Eur Spine J 2009, 18:1001-1007. 10.1007/s00586-009-0940-x, 2899582, 19308465.
11. Kato K, Kikuchi S, Konno S, Sekiguchi M. Participation of 5-hydroxytryptamine in pain-related behavior induced by nucleus pulposus applied on the nerve root in rats. Spine (Phila Pa 1976) 2008, 33:1330-1336.
12. Onda A, Murata Y, Rydevik B, Larsson K, Kikuchi S, Olmarker K. Nerve growth factor content in dorsal root ganglion as related to changes in pain behavior in a rat model of experimental lumbar disc herniation. Spine (Phila Pa 1976) 2005, 30:188-193.
13. Cuellar JM, Montesano PX, Carstens E. Role of TNF-alpha in sensitization of nociceptive dorsal horn neurons induced by application of nucleus pulposus to L5 dorsal root ganglion in rats. Pain 2004, 110:578-587. 10.1016/j.pain.2004.03.029, 15288398.
14. Ito T, Ohtori S, Inoue G, Koshi T, Doya H, Ozawa T, Saito T, Moriya H, Takahashi K. Glial phosphorylated p38 MAP kinase mediates pain in a rat model of lumbar disc herniation and induces motor dysfunction in a rat model of lumbar spinal canal stenosis. Spine (Phila Pa 1976) 2007, 32:159-167.
15. Igarashi T, Kikuchi S, Shubayev V, Myers RR. 2000 Volvo Award winner in basic science studies: Exogenous tumor necrosis factor-alpha mimics nucleus pulposus-induced neuropathology. Molecular, histologic, and behavioral comparisons in rats. Spine (Phila Pa 1976) 2000, 25:2975-2980.
16. Rutkowski MD, DeLeo JA. The Role of Cytokines in the Initiation and Maintenance of Chronic Pain. Drug News Perspect 2002, 15:626-632. 10.1358/dnp.2002.15.10.740239, 12677247.
17. Kang JD, Georgescu HI, McIntyre-Larkin L, Stefanovic-Racic M, Donaldson WF, Evans CH. Herniated lumbar intervertebral discs spontaneously produce matrix metalloproteinases, nitric oxide, interleukin-6, and prostaglandin E2. Spine (Phila Pa 1976) 1996, 21:271-277.
18. Weiler C, Nerlich AG, Bachmeier BE, Boos N. Expression and distribution of tumor necrosis factor alpha in human lumbar intervertebral discs: a study in surgical specimen and autopsy controls. Spine (Phila Pa 1976) 2005, 30:44-53. discussion 54.
19. Takahashi N, Kikuchi S, Shubayev VI, Campana WM, Myers RR. TNF-alpha and phosphorylation of ERK in DRG and spinal cord: insights into mechanisms of sciatica. Spine (Phila Pa 1976) 2006, 31:523-529.
20. Ohtori S, Takahashi K, Moriya H, Myers RR. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord. Spine (Phila Pa 1976) 2004, 29:1082-1088.
21. Shubayev VI, Myers RR. Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors. J Neuroimmunol 2001, 114:48-56. 10.1016/S0165-5728(00)00453-7, 11240015.
22. Sweitzer SM, Hickey WF, Rutkowski MD, Pahl JL, DeLeo JA. Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: potential relationship to neuropathic pain. Pain 2002, 100:163-170. 10.1016/S0304-3959(02)00257-9, 12435469.
23. Ozaktay AC, Cavanaugh JM, Asik I, DeLeo JA, Weinstein JN. Dorsal root sensitivity to interleukin-1 beta, interleukin-6 and tumor necrosis factor in rats. Eur Spine J 2002, 11:467-475. 10.1007/s00586-002-0430-x, 12384756.
24. Ozaktay AC, Kallakuri S, Takebayashi T, Cavanaugh JM, Asik I, DeLeo JA, Weinstein JN. Effects of interleukin-1 beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur Spine J 2006, 15:1529-1537. 10.1007/s00586-005-0058-8, 16474945.
25. Kawaguchi S, Yamashita T, Yokogushi K, Murakami T, Ohwada O, Sato N. Immunophenotypic analysis of the inflammatory infiltrates in herniated intervertebral discs. Spine (Phila Pa 1976) 2001, 26:1209-1214.
26. Winkelstein BA, Rutkowski MD, Sweitzer SM, Pahl JL, DeLeo JA. Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression but differential behavioral responses to pharmacologic treatment. J Comp Neurol 2001, 439:127-139. 10.1002/cne.2000, 11596043.
27. Rothman SM, Huang Z, Lee KE, Weisshaar CL, Winkelstein BA. Cytokine mRNA expression in painful radiculopathy. J Pain 2009, 10:90-99. 10.1016/j.jpain.2008.07.008, 2630380, 18848809.
28. Rothman SM, Winkelstein BA. Cytokine antagonism reduces pain and modulates spinal astrocytic reactivity after cervical nerve root compression. Ann Biomed Eng 2010, 38:2563-2576. 10.1007/s10439-010-0012-8, 20309734, 20309734.
29. DeLeo JA, Colburn RW, Rickman AJ. Cytokine and growth factor immunohistochemical spinal profiles in two animal models of mononeuropathy. Brain Res 1997, 759:50-57. 10.1016/S0006-8993(97)00209-6, 9219862.
30. Wajant H, Pfizenmaier K, Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 2003, 10:45-65. 10.1038/sj.cdd.4401189, 12655295.
31. Zhang L, Berta T, Xu ZZ, Liu T, Park JY, Ji RR. TNF-alpha contributes to spinal cord synaptic plasticity and inflammatory pain: distinct role of TNF receptor subtypes 1 and 2. Pain 2011, 152:419-427. 10.1016/j.pain.2010.11.014, 21159431.
32. Sweitzer S, Martin D, DeLeo JA. Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience 2001, 103:529-539. 10.1016/S0306-4522(00)00574-1, 11246166.
33. Sommer C, Schmidt C, George A. Hyperalgesia in experimental neuropathy is dependent on the TNF receptor 1. Exp Neurol 1998, 151:138-142. 10.1006/exnr.1998.6797, 9582261.
34. Sinclair SM, Shamji MF, Chen J, Jing L, Richardson WJ, Brown CR, Fitch RD, Setton LA. Attenuation of Inflammatory events in human intervertebral disc cells with a tumor necrosis factor antagonist. Spine (Phila Pa 1976) 2011, 36:1190-1196.
35. Kato K, Kikuchi S, Shubayev VI, Myers RR. Distribution and tumor necrosis factor-alpha isoform binding specificity of locally administered etanercept into injured and uninjured rat sciatic nerve. Neuroscience 2009, 160:492-500. 10.1016/j.neuroscience.2009.02.038, 19250961.
36. Korhonen T, Karppinen J, Paimela L, Malmivaara A, Lindgren KA, Bowman C, Hammond A, Kirkham B, Jarvinen S, Niinimaki J, Veeger N, Haapea M, Torkki M, Tervonen O, Seitsalo S, Hurri H. The treatment of disc-herniation-induced sciatica with infliximab: one-year follow-up results of FIRST II, a randomized controlled trial. Spine (Phila Pa 1976) 2006, 31:2759-2766.
37. Korhonen T, Karppinen J, Paimela L, Malmivaara A, Lindgren KA, Jarvinen S, Niinimaki J, Veeger N, Seitsalo S, Hurri H. The treatment of disc herniation-induced sciatica with infliximab: results of a randomized, controlled, 3-month follow-up study. Spine (Phila Pa 1976) 2005, 30:2724-2728.
38. Cohen SP, Bogduk N, Dragovich A, Buckenmaier CC, Griffith S, Kurihara C, Raymond J, Richter PJ, Williams N, Yaksh TL. Randomized, double-blind, placebo-controlled, dose-response, and preclinical safety study of transforaminal epidural etanercept for the treatment of sciatica. Anesthesiology 2009, 110:1116-1126. 10.1097/ALN.0b013e3181a05aa0, 19387178.
39. van Wilgen CP, Stewart R, Patrick Stegeman PT, Coppes M, van Wijhe M. Fear of movement in pre-operative patients with a lumbar stenosis and or herniated disc: Factor structure of the Tampa scale for kinesiophobia. Man Ther 2010, 15:593-598. 10.1016/j.math.2010.07.002, 20705501.
40. Winter CC, Brandes M, Muller C, Schubert T, Ringling M, Hillmann A, Rosenbaum D, Schulte TL. Walking ability during daily life in patients with osteoarthritis of the knee or the hip and lumbar spinal stenosis: a cross sectional study. BMC Musculoskelet Disord 2010, 11:233. 10.1186/1471-2474-11-233, 2958990, 20939866.
41. Lee JH, An JH, Lee SH, Seo IS. Three-dimensional gait analysis of patients with weakness of ankle dorsiflexor as a result of unilateral L5 radiculopathy. J Back Musculoskelet Rehabil 2010, 23:49-54.
42. Mogil JS, Graham AC, Ritchie J, Hughes SF, Austin JS, Schorscher-Petcu A, Langford DJ, Bennett GJ. Hypolocomotion, asymmetrically directed behaviors (licking, lifting, flinching, and shaking) and dynamic weight bearing (gait) changes are not measures of neuropathic pain in mice. Mol Pain 6:34.
43. Hedrick T. DLTdataviewer. Chapel Hill, NC., http://www.unc.edu/~thedrick/software1.html
44. Allen KD, Griffin TM, Rodriguiz RM, Wetsel WC, Kraus VB, Huebner JL, Boyd LM, Setton LA. Decreased physical function and increased pain sensitivity in mice deficient for type IX collagen. Arthritis Rheum 2009, 60:2684-2693. 10.1002/art.24783, 2760314, 19714629.
45. Hildebrand M. The quadrupedal gaits of vertebrates: the timing of leg movements relates to balance, body shape, agility, speed, and energy expenditure. BioScience 1989, 39:766-775.
46. Zumwalt AC, Hamrick M, Schmitt D. Force plate for measuring the ground reaction forces in small animal locomotion. J Biomech 2006, 39:2877-2881. 10.1016/j.jbiomech.2005.10.006, 16356506.
47. Howard CS, Blakeney DC, Medige J, Moy OJ, Peimer CA. Functional assessment in the rat by ground reaction forces. J Biomech 2000, 33:751-757. 10.1016/S0021-9290(00)00023-3, 10807997.
48. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63. 10.1016/0165-0270(94)90144-9, 7990513.
49. Deleo TA, Hashizume H, Rutkowski MD, Weinstein TN. Cyclooxygenase-2 inhibitor SC-236 attenuates mechanical allodynia following nerve root injury in rats. J Orthop Res 2000, 18:977-982. 10.1002/jor.1100180618, 11192259.
50. Hashizume H, Rutkowski MD, Weinstein JN, DeLeo JA. Central administration of methotrexate reduces mechanical allodynia in an animal model of radiculopathy/sciatica. Pain 2000, 87:159-169. 10.1016/S0304-3959(00)00281-5, 10924809.
51. Hashizume H, DeLeo JA, Colburn RW, Weinstein JN. Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine (Phila Pa 1976) 2000, 25:1206-1217.
52. Zhang KB, Zheng ZM, Liu H, Liu XG. The effects of punctured nucleus pulposus on lumbar radicular pain in rats: a behavioral and immunohistochemical study. J Neurosurg Spine 2009, 11:492-500. 10.3171/2009.4.SPINE08744, 19929348.
53. Lee SJ, Han TR, Hyun JK, Jeon JY, Myong NH. Electromyographic findings in nucleus pulposus-induced radiculopathy in the rat. Spine (Phila Pa 1976) 2006, 31:2053-2058.
54. Olmarker K, Iwabuchi M, Larsson K, Rydevik B. Walking analysis of rats subjected to experimental disc herniation. Eur Spine J 1998, 7:394-399. 10.1007/s005860050096, 9840473.
55. Allen KD, Adams SB, Mata BA, Shamji MF, Gouze E, Jing L, Nettles DL, Latt LD, Setton LA. Gait and behavior in an IL-1β-mediated model of rat knee arthritis and effects of an IL1 antagonist. J Orthop Res 2011, 29:694-703. 10.1002/jor.21309, 21437948.
56. Allen KD, Adams SB, Setton LA. Evaluating intra-articular drug delivery for the treatment of osteoarthritis in a rat model. Tissue Eng Part B Rev 2010, 16:81-92. 2817653, 19943805.
57. Schneider E, Chao EY. Fourier analysis of ground reaction forces in normals and patients with knee joint disease. J Biomech 1983, 16:591-601. 10.1016/0021-9290(83)90109-4, 6643531.
58. Deumens R, Jaken RJ, Marcus MA, Joosten EA. The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J Neurosci Methods 2007, 164:120-130. 10.1016/j.jneumeth.2007.04.009, 17532474.
59. Koopmans GC, Deumens R, Honig WM, Hamers FP, Steinbusch HW, Joosten EA. The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J Neurotrauma 2005, 22:214-225. 10.1089/neu.2005.22.214, 15716628.
60. Murata Y, Rydevik B, Takahashi K, Takahashi I, Olmarker K. Macrophage appearance in the epineurium and endoneurium of dorsal root ganglion exposed to nucleus pulposus. J Peripher Nerv Syst 2004, 9:158-164. 10.1111/j.1085-9489.2004.09305.x, 15363063.