Topical high molecular weight hyaluronan reduces radicular pain post laminectomy in a rat model

Spine Journal

Volumn 5, Issue 5, 2005, Pages 494-502

  Massie, Jennifer B ^a   Schimizzi, Aimee L ^a   Huang, Bill ^a   Kim, Choll W ^a   Garfin, Steven R ^a   Akeson, Wayne H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Disc injury; Epidural fibrosis; HA gel; Laminectomy; Spine; Tactile allodynia

Indexed keywords

COLLAGEN; HYALURONIC ACID; HYDROXYPROLINE;

ANALYSIS OF VARIANCE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FIBROSIS; FISHER EXACT TEST; LAMINECTOMY; LUMBAR SPINE; MALE; NONHUMAN; PAIN ASSESSMENT; POSTOPERATIVE PAIN; PRIORITY JOURNAL; PROTEIN CONTENT; QUANTITATIVE ANALYSIS; RADICULAR PAIN; RAT; SCAR FORMATION; SENSITIVITY ANALYSIS; SPINAL NERVE; STATISTICAL SIGNIFICANCE; TOUCH;

ADMINISTRATION, TOPICAL; ANIMALS; CICATRIX; GELS; HYALURONIC ACID; LAMINECTOMY; LUMBAR VERTEBRAE; MALE; MOLECULAR WEIGHT; PAIN MEASUREMENT; PAIN, POSTOPERATIVE; RATS; RATS, SPRAGUE-DAWLEY; SPINAL NERVE ROOTS; SPINAL NERVES;

EID: 24644511805     PISSN: 15299430     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.spinee.2004.12.003     Document Type: Article

References (98)

1. J. Cauchoix C. Ficat B. Girard Repeat surgery after disc excision Spine 3 1978 256-9
2. C.V. Burton Lumbosacral arachnoiditis Spine 3 1978 24-30
3. U. Ebeling H. Kalbarcyk H.J. Reulen [Microsurgery reinterventions following lumbar intervertebral disk surgery. Results and prognosis] Nervenarzt 60 1989 553-8
4. B. Jonsson B. Stromqvist Repeat decompression of lumbar nerve roots: A prospective two-year evaluation J Bone Joint Surg Br 75 1993 894-7
5. R.B. North J.N. Campbell C.S. James et al. Failed back surgery syndrome: 5-year follow-up in 102 patients undergoing repeated operation Neurosurgery 28 1991 685-90 discussion 90-1
6. J. Key L. Ford Experimental intervertebral disc lesions J Bone Joint Surg 30 1948 621-30
7. C.A. Fager S.R. Freidberg Analysis of failures and poor results of lumbar spine surgery Spine 5 1980 87-94
8. H. Pheasant Sources of failure in laminectomies Orthop Clin North Am 6 1975 319-29
9. N. de Tribolet F. Porchet T.W. Lutz et al. Clinical assessment of a novel antiadhesion barrier gel: Prospective, randomized, multicenter, clinical trial of ADCON-L to inhibit postoperative peridural fibrosis and related symptoms after lumbar discectomy Am J Orthopaed 27 1998 111-20
10. J.P. Vogelsang M. Finkenstaedt M. Vogelsang E. Markakis Recurrent pain after lumbar discectomy: The diagnostic value of peridural scar on MRI Eur Spine J 8 1999 475-9
11. E. Coskun T. Suzer O. Topuz M. Zencir E. Pakdemirli K. Tahta Relationships between epidural fibrosis, pain, disability, and psychological factors after lumbar disc surgery Eur Spine J 9 2000 218-23
12. M. Annertz B. Jonsson B. Stromqvist S. Holtas Serial MRI in the early postoperative period after lumbar discectomy Neuroradiology 37 1995 177-82
13. J.W. Van Goethem E. Van de Kelft I.G. Biltjes et al. MRI after successful lumbar discectomy Neuroradiology 38 Suppl. 1 1996 S90-6
14. K.M. Bullard D.L. Cass M.J. Banda N.S. Adzick Transforming growth factor beta-1 decreases interstitial collagenase in healing human fetal skin J Pediatr Surg 32 1997 1023-7
15. V.S. Mehta A.K. Banerji R.P. Tripathi Surgical treatment of brachial plexus injuries Br J Neurosurg 7 1993 491-500
16. N.S. Adzick H.P. Lorenz Cells, matrix, growth factors, and the surgeon: the biology of scarless fetal wound repair Ann Surg 220 1994 10-8
17. C. Belluco F. Meggiolaro D. Pressato et al. Prevention of postsurgical adhesions with an autocrosslinked hyaluronan derivative gel J Surg Res 100 2001 217-21
18. J.W. Burns M.J. Colt L.S. Burgees K.C. Skinner Preclinical evaluation of Seprafilm bioresorbable membrane Eur J Surg Suppl 577 1997 40-8
19. B. Haslinger S. Mandl-Weber A. Sellmayer T. Sitter Hyaluronan fragments induce the synthesis of MCP-1 and IL-8 in cultured human peritoneal mesothelial cells Cell Tissue Res 305 2001 79-86
20. B.W. Hellebrekers G.C. Trimbos-Kemper C.A. van Blitterswijk E.A. Bakkum J.B. Trimbos Effects of five different barrier materials on postsurgical adhesion formation in the rat Hum Reprod 15 2000 1358-63
21. K. Rodgers D. Cohn A. Hotovely E. Pines M.P. Diamond G. diZerega Evaluation of polyethylene glycol/polylactic acid films in the prevention of adhesions in the rabbit adhesion formation and reformation sidewall models Fertil Steril 69 1998 403-8
22. A. Jacob B.T. Faddis R.A. Chole MeroGel hyaluronic acid sinonasal implants: Osteogenic implications Laryngoscope 112 2002 37-42
23. C.P. Kimmelman D.R. Edelstein H.J. Cheng Sepragel sinus (hylan B) as a postsurgical dressing for endoscopic sinus surgery Otolaryngol Head Neck Surg 125 2001 603-8
24. D. McIntosh A. Cowin D. Adams T. Rayner P.J. Wormald The effect of a dissolvable hyaluronic acid-based pack on the healing of the nasal mucosa of sheep Am J Rhinol 16 2002 85-90
25. K. Takahashi J. Takeuchi T. Takahashi S. Miyauchi K. Horie Y. Uchiyama Effects of sodium hyaluronate on epithelial healing of the vesical mucosa and vesical fibrosis in rabbits with acetic acid induced cystitis J Urol 166 2001 710-3
26. J.L. Hinton Jr. D.J. Warejcka Y. Mei et al. Inhibition of epidural scar formation after lumbar laminectomy in the rat Spine 20 1995 564-70 discussion 79-80
27. FDA Review of Adcon-L. Wall Street Journal, p. B11, August 31, 2000.
28. J. Brotchi B. Pirotte O. De Witte M. Levivier Prevention of epidural fibrosis in a prospective series of 100 primary lumbo-sacral discectomy patients: Follow-up and assessment at re-operation Neurol Res 21 1999 S47-50
29. N. de Tribolet J.T. Robertson Lack of postdiscectomy adhesions following application of ADCON-L: A case report Eur Spine J 5 1996 S18-20
30. N. deTribolet F. Porchet T. Lutz et al. Clinical assessment of a novel anti-adhesion barrier gel prospective randomized multicenter clinical trial of ADCON-L to inhibit postoperative peridural fibrosis and related symptoms after lumbar discectomy Am J Orthopaed 27 1998 111-20
31. S.L. Einhaus J.T. Robertson F.C. Dohan Jr. J.R. Wujek S. Ahmad Reduction of peridural fibrosis after lumbar laminotomy and discectomy in dogs by a resorbable gel (ADCON-L) Spine 22 1997 1440-6 discussion 6-7
32. R.C. Frederickson ADCON-L: A review of its development, mechanism of action, and preclinical data Eur Spine J 5 1996 S7-9
33. A.X. Le D.E. Rogers E.G. Dawson M.A. Kropf D.A. De Grange R.B. Delamarter Unrecognized durotomy after lumbar discectomy: A report of four cases associated with the use of ADCON-L Spine 26 2001 115-7 discussion 8
34. L.D. Hieb D.L. Stevens Spontaneous postoperative cerebrospinal fluid leaks following application of anti-adhesion barrier gel: Case report and review of the literature Spine 26 2001 748-51
35. J.C. Maroon A. Abla J. Bost Association between peridural scar and persistent low back pain after lumbar discectomy Neurol Res 21 1999 S43-6
36. D. McKinley L. Schaffer Cost effectiveness evaluation of ADCON-L adhesion control gel in lumbar surgery Neurol Res 21 1999 s67-71
37. F. Porchet D. Lombardi J. de Preux I.K. Pople Inhibition of epidural fibrosis with ADCON-L: Effect on clinical outcome one year following re-operation for recurrent lumbar radiculopathy Neurol Res 21 1999 S51-60
38. J.T. Robertson J.L. Petrie R.C. Frederickson N. de Tribolet R. Hardy ADCON-L symposium. Round table discussion Eur Spine J 5 1996 S26-8
39. J.T. Robertson K. Maier R.W. Anderson J.L. Mule E.A. Palatinsky Prevention of epidural fibrosis with ADCON-L in presence of a durotomy during lumbar disc surgery: Experiences with a pre-clinical model Neurol Res 21 1999 S61-6
40. J. Ross J. Robertson R. Frederickson et al. Association between peridural scar and recurrent radicular pain after lumbar discectomy: magnetic resonance evaluation. ADCON-L European Study Group Neurosurgery 38 1996 855-61
41. J.S. Ross N. Obuchowski M.T. Modic MR evaluation of epidural fibrosis: proposed grading system with intra- and inter-observer variability Neurol Res 21 1999 S23-6
42. D. Schwicker Cost effectiveness of lumbar disc surgery and of a preventive treatment for peridural fibrosis Eur Spine J 5 1996 S21-5
43. M.N. Songer L. Ghosh D.L. Spencer Effects of sodium hyaluronate on peridural fibrosis after lumbar laminotomy and discectomy Spine 15 1990 550-4
44. F.M. Amara J. Entwistle T.I. Kuschak E.A. Turley J.A. Wright Transforming growth factor-beta1 stimulates multiple protein interactions at a unique cis-element in the 3′-untranslated region of the hyaluronan receptor RHAMM mRNA J Biol Chem 271 1996 15279-84
45. E. Balazs B. Jacobson The chemistry and biology of compounds containing amino sugars In: E. Balazs R. Jeanlo, eds. The amino sugars 1966 Academic Press New York and London 386
46. E. Balazs Z. Darzynkiewicz The effect of HA on fibroblasts, mononuclear phagocytes and lymphocytes In: E. Kulonen K. Pikkaraihen eds. Biology of the fibroblast 1973 Academic Press London, New York 237-262
47. M.I. Tammi A.J. Day E.A. Turley Hyaluronan and homeostasis: A balancing act J Biol Chem 277 2002 4581-4584
48. B.P. Toole T.N. Wight M.I. Tammi Hyaluronan-cell interactions in cancer and vascular disease J Biol Chem 277 2002 4593-4596
49. M. Yasuda K. Nakano K. Yasumoto Y. Tanaka CD44: Functional relevance to inflammation and malignancy Histol Histopathol 17 2002 945-950
50. R.C. Savani G. Cao P.M. Pooler A. Zaman Z. Zhou H.M. DeLisser Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis J Biol Chem 276 2001 36770-36778
51. K.M. Bullard M.T. Longaker H.P. Lorenz Fetal wound healing: Current biology World J Surg 27 2003 54-61
52. S. Zhang M.C. Chang D. Zylka S. Turley R. Harrison E.A. Turley The hyaluronan receptor RHAMM regulates extracellular-regulated kinase J Biol Chem 273 1998 11342-11348
53. A. Rossler H. Hinghofer-Szalkay Hyaluronan fragments: An information-carrying system? Horm Metab Res 35 2003 67-68
54. J. Cichy E. Pure The liberation of CD44 J Cell Biol 161 2003 839-843
55. P. Ghosh D. Guidolin Potential mechanism of action of intra-articular hyaluronan therapy in osteoarthritis: Are the effects molecular weight dependent? Semin Arthritis Rheum 32 2002 10-37
56. P.H. Weigel J.H. Yik Glycans as endocytosis signals: The cases of the asialoglycoprotein and hyaluronan/chondroitin sulfate receptors Biochim Biophys Acta 1572 2002 341-363
57. S. Alaish D. Yager R. Diegelmann I. Cohen Biology of fetal wound healing: Hyaluronate receptor expression in fetal fibroblasts J Pediatr Surg 29 1994 1040-1043
58. Ferguson Skin wound healing. Transforming growth factor beta antagonists decrease scarring and improve quality J Interferon Res 14 1994 303-304
59. R.M. Greco J.A. Iocono H.P. Ehrlich Hyaluronic acid stimulates human fibroblast proliferation within a collagen matrix J Cell Physiol 177 1998 465-473
60. Massie JB, Yaksh TL, Kim CW, Garfin SR, Akeson WH. A post-laminectomy rat model mimics the Chung tactile allodynia model. Paper presented at the 49th Annual Meeting of the Orthopaedic Research Society, New Orleans, LA, February 2-5, 2003.
61. P.W. Noble Hyaluronan and its catabolic products in tissue injury and repair Matrix Biol 21 2002 25-29
62. T.C. Laurent J.R. Fraser Hyaluronan FASEB J 6 1992 2397-2404
63. H. Kobayashi M. Suzuki N. Kanayama T. Nishida M. Takigawa T. Terao CD44 stimulation by fragmented hyaluronic acid induces upregulation of urokinase-type plasminogen activator and its receptor and subsequently facilitates invasion of human chondrosarcoma cells Int J Cancer 102 2002 379-389
64. M. Slevin S. Kumar J. Gaffney Angiogenic oligosaccharides of hyaluronan induce multiple signaling pathways affecting vascular endothelial cell mitogenic and wound healing responses J Biol Chem 277 2002 41046-41059
65. B. Dube H.J. Luke M. Aumailley P. Prehm Hyaluronan reduces migration and proliferation in CHO cells Biochim Biophys Acta 1538 2001 283-289
66. R.L. Goldberg B.P. Toole Hyaluronate inhibition of cell proliferation Arthritis Rheum 30 1987 769-778
67. Y. Tanaka Y. Makiyama Y. Mitsui Endothelin-1 is involved in the growth promotion of vascular smooth muscle cells by hyaluronic acid Int J Cardiol 76 2000 39-47
68. K.M. Sheehan L.B. DeLott S.M. Day D.H. DeHeer Hyalgan has a dose-dependent differential effect on macrophage proliferation and cell death J Orthop Res 21 2003 744-751
69. A. Sattar P. Rooney S. Kumar et al. Application of angiogenic oligosaccharides of hyaluronan increases blood vessel numbers in rat skin J Invest Dermatol 103 1994 576-579
70. C.M. McKee M.B. Penno M. Cowman et al. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44 J Clin Invest 98 1996 2403-2413
71. A. Nandi P. Estess M.H. Siegelman Hyaluronan anchoring and regulation on the surface of vascular endothelial cells is mediated through the functionally active form of CD44 J Biol Chem 275 2000 14939-14948
72. D. Naot R.V. Sionov D. Ish-Shalom CD44: Structure, function, and association with the malignant process Adv Cancer Res 71 1997 241-319
73. J. Lesley V.C. Hascall M. Tammi R. Hyman Hyaluronan binding by cell surface CD44 J Biol Chem 275 2000 26967-26975
74. G. Borland J.A. Ross K. Guy Forms and functions of CD44 Immunology 93 1998 139-148
75. Y. Fujita M. Kitagawa S. Nakamura et al. CD44 signaling through focal adhesion kinase and its anti-apoptotic effect FEBS Lett 528 2002 101-108
76. C.M. Isacke H. Yarwood The hyaluronan receptor, CD44 Int J Biochem Cell Biol 34 2002 718-721
77. G.J. Bennett An animal model of neuropathic pain: A review Muscle Nerve 16 1993 1040-1048
78. S.M. Carlton H.A. Lekan S.H. Kim J.M. Chung Behavioral manifestations of an experimental model for peripheral neuropathy produced by spinal nerve ligation in the primate Pain 56 1994 155-166
79. J.A. DeLeo D.W. Coombs S. Willenbring R.W. Colburn C. Fromm R. Wagner B.B. Twitchell Characterization of a neuropathic pain model: Sciatic cryoneurolysis in the rat Pain 56 1994 9-16
80. P. Honore S.D. Rogers M.J. Schwei et al. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons Neuroscience 98 2000 585-598
81. S.R. Chaplan F.W. Bach J.W. Pogrel J.M. Chung T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci Methods 53 1994 55-63
82. J.F. Woessner Jr. R.I. Bashey R.J. Boucek Collagen development in heart and skin of the chick embryo Biochim Biophys Acta 140 1967 329-338
83. J. Abitbol T. Lincoln B. Lind D. Amiel W. Akeson S. Garfin Preventing postlaminectomy adhesion: A new experimental model Spine 19 1994 1809-1814
84. R.W. Colburn J.A. DeLeo A.J. Rickman M.P. Yeager P. Kwon W.F. Hickey Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat J Neuroimmunol 79 1997 163-175
85. K. Olmarker M. Nutu R. Storkson Changes in spontaneous behavior in rats exposed to experimental disc herniation are blocked by selective TNF-alpha inhibition Spine 28 2003 1635-1641
86. Y. Shir R. Zeltser J.J. Vatine et al. Correlation of intact sensibility and neuropathic pain-related behaviors in eight inbred and outbred rat strains and selection lines Pain 90 2001 75-82
87. R. Wagner R.R. Myers Endoneurial injection of TNF-alpha produces neuropathic pain behaviors Neuroreport 7 1996 2897-2901
88. T.L. Yaksh X.Y. Hua I. Kalcheva N. Nozaki-Taguchi M. Marsala The spinal biology in humans and animals of pain states generated by persistent small afferent input Proc Natl Acad Sci U S A 96 1999 7680-7686
89. D.C. West I.N. Hampson F. Arnold S. Kumar Angiogenesis induced by degradation products of hyaluronic acid Science 228 1985 1324-1326
90. H. Xu A. Manivannan J. Liversidge P.F. Sharp J.V. Forrester I.J. Crane Involvement of CD44 in leukocyte trafficking at the blood-retinal barrier J Leukoc Biol 72 2002 1133-1141
91. M.E. Mummert M. Mohamadzadeh D.I. Mummert N. Mizumoto A. Takashima Development of a peptide inhibitor of hyaluronan-mediated leukocyte trafficking J Exp Med 192 2000 769-779
92. T. Habara M. Nakatsuka H. Konishi K. Asagiri S. Noguchi T. Kudo The biological effects of antiadhesion agents on activated RAW264.7 macrophages J Biomed Mater Res 61 2002 628-633
93. M. Slevin J. Krupinski S. Kumar J. Gaffney Angiogenic oligosaccharides of hyaluronan induce protein tyrosine kinase activity in endothelial cells and activate a cytoplasmic signal transduction pathway resulting in proliferation Lab Invest 78 1998 987-1003
94. E.A. Balazs J.L. Denlinger Clinical uses of hyaluronan Ciba Found Symp 143 1989 265-275
95. N. Liu L. Shao X. Xu et al. Hyaluronan metabolism in rat tail skin following blockage of the lymphatic circulation Lymphology 35 2002 15-22
96. J. Fraser T. Laurent U. Laurent Hyaluron: Its nature, distribution, functions and turnover J Intern Med 242 1997 27-33
97. A. Lindholm B. Roneus G. Lindblad B. Jones Hyaluronan turnover in the synovial fluid in metacarpophalangeal and middle carpal joints in standardbred horses Acta Vet Scand 37 1996 147-151
98. P.W. Mantyh D.R. Clohisy M. Koltzenburg S.P. Hunt Molecular mechanisms of cancer pain Nat Rev Cancer 2 2002 201-209