Tissue engineering strategies applied in the regeneration of the human intervertebral disk

Biotechnology Advances

Volumn 31, Issue 8, 2013, Pages 1514-1531

  Silva Correia, Joana ^a   Correia, Sandra I ^a   Oliveira, Joaquim M ^a   Reis, Rui L ^a  

^a UNIVERSITY OF MINHO   (Portugal)

Author keywords

Degeneration; Intervertebral disk; Regeneration; Spinal disorder; Spinal surgery; Tissue engineering

Indexed keywords

DEGENERATION; INTERVERTEBRAL DISK; REGENERATION; SPINAL DISORDERS; SPINAL SURGERY;

CARTILAGE; PATHOLOGY; SURGERY; TISSUE; TISSUE ENGINEERING;

TISSUE REGENERATION;

DISEASE; HEALTH RISK; MEDICINE; PATHOLOGY; REGENERATION; RESEARCH AND DEVELOPMENT;

TISSUE SCAFFOLD;

ANIMAL; CYTOLOGY; DEGENERATION; HUMAN; INTERVERTEBRAL DISK; MOUSE; PERCUTANEOUS VERTEBROPLASTY; PHYSIOLOGY; RABBIT; RAT; REGENERATION; REVIEW; SPINAL DISORDER; SPINE SURGERY; TISSUE ENGINEERING;

DEGENERATION; INTERVERTEBRAL DISK; REGENERATION; SPINAL DISORDER; SPINAL SURGERY; TISSUE ENGINEERING;

ANIMALS; HUMANS; INTERVERTEBRAL DISC; MICE; RABBITS; RATS; REGENERATION; TISSUE ENGINEERING; TISSUE SCAFFOLDS; VERTEBROPLASTY;

EID: 84888012852     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2013.07.010     Document Type: Review

References (188)

1. Adams M.A., Roughley P.J. What is intervertebral disc degeneration, and what causes it?. Spine (Phila Pa 1976) 2006, 31:2151-2161.
2. Ahmadi R., Burns A.J., de Bruijn J.D. Chitosan-based hydrogels do not induce angiogenesis. J Tissue Eng Regen Med 2010, 4:309-315.
3. Ahrens M., Tsantrizos A., Donkersloot P., Martens F., Lauweryns P., Le Huec J.C., et al. Nucleus replacement with the DASCOR disc arthroplasty device: interim two-year efficacy and safety results from two prospective, non-randomized multicenter European studies. Spine 2009, 34:1376-1384.
4. Akeda K., An H.S., Pichika R., Attawia M., Thonar E.J., Lenz M.E., et al. Platelet-rich plasma (PRP) stimulates the extracellular matrix metabolism of porcine nucleus pulposus and anulus fibrosus cells cultured in alginate beads. Spine 2006, 31:959-966.
5. Alleyne C.H., Rodts G.E. Current and future approaches to lumbar disc surgery (a literature review). Med Gen Med 1997, 1:1-14.
6. Ambrosio L., Netti P.A., Iannace S., Huang S.J., Nicolais L. Composite hydrogels for intervertebral disc prostheses. J Mater Sci Mater Med 1996, 7:251-254.
7. Andersson G.B.J. Epidemiological features of chronic low-back pain. Lancet 1999, 354:581-585.
8. Azzazi A., AlMekawi S., Zein M. Lumbar disc nucleoplasty using coblation technology: clinical outcome. J Neurointerv Surg 2011, 3:288-292.
9. Bae W.C., Masuda K. Emerging technologies for molecular therapy for intervertebral disk degeneration. Orthop Clin North Am 2011, 42:585-601.
10. Baer A.E., Wang J.Y., Kraus V.B., Setton L.A. Collagen gene expression and mechanical properties of intervertebral disc cell-alginate cultures. J Orthop Res 2001, 19:2-10.
11. Barrey C.Y., Ponnappan R.K., Song J., Vaccaro A.R. Biomechanical evaluation of pedicle screw-based dynamic stabilization devices for the lumbar spine: a systematic review. SAS J 2008, 2:159-170.
12. Battié M.C., Videman T., Kaprio J., Gibbons L.E., Gill K., Manninen H., et al. The Twin Spine Study: contributions to a changing view of disc degeneration. Spine J 2009, 9:47-59.
13. Battié M.C., Videman T., Parent E. Lumbar disc degeneration: epidemiology and genetic influences. Spine 2004, 29:2679-2690.
14. Berger J., Reist M., Mayer J.M., Felt O., Gurny R. Structure and interactions in chitosan hydrogels formed by complexation or aggregation for biomedical applications. Eur J Pharm Biopharm 2004, 57:35-52.
15. Berger J., Reist M., Mayer J.M., Felt O., Peppas N.A., Gurny R. Structure and interactions in covalently and ionically crosslinked chitosan hydrogels for biomedical applications. Eur J Pharm Biopharm 2004, 57:19-34.
16. Bertolo A., Ettinger L., Aebli N., Haschtmann D., Baur M., Berlemann U., et al. The in vitro effects of dexamethasone, insulin and triiodothyronine on degenerative human intervertebral disc cells under normoxic and hypoxic conditions. Eur Cell Mater 2011, 21:221-229.
17. Bibby S.R.S., Urban J.P.G. Effect of nutrient deprivation on the viability of intervertebral disc cells. Eur Spine J 2004, 13:695-701.
18. Blanco J.F., Graciani I.F., Sanchez-Guijo F.M., Muntión S., Hernandez-Campo P., Santamaria C., et al. Isolation and characterization of mesenchymal stromal cells from human degenerated nucleus pulposus: comparison with bone marrow mesenchymal stromal cells from the same subjects. Spine 2010, 35:2259-2265.
19. Bono C.M., Garfin S.R. History and evolution of disc replacement. Spine J 2004, 4:S145-S150.
20. Boos N., Weissbach S., Rohrbach H., Weiler C., Spratt K.F., Nerlich A.G. Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in Basic Science. Spine 2002, 27:2631-2644.
21. Boyd L., Carter A. Injectable biomaterials and vertebral endplate treatment for repair and regeneration of the intervertebral disc. Eur Spine J 2006, 15:414-421.
22. Brisby H., Papadimitriou N., Brantsing C., Bergh P., Lindahl A., Henriksson H.B. The presence of local mesenchymal progenitor cells in human degenerated intervertebral discs and possibilities to influence these in vitro: a descriptive study in humans. Stem Cells Dev 2013, 22:804-814.
23. Bron J., Helder M., Meisel H.-J., Van Royen B., Smit T. Repair, regenerative and supportive therapies of the annulus fibrosus: achievements and challenges. Eur Spine J 2009, 18:301-313.
24. Bron J.L., Vonk L.A., Smit T.H., Koenderink G.H. Engineering alginate for intervertebral disc repair. J Mech Behav Biomed Mater 2011, 4:1196-1205.
25. Bryant S.J., Anseth K.S. Controlling the spatial distribution of ECM components in degradable PEG hydrogels for tissue engineering cartilage. J Biomed Mater Res A 2003, 64A:70-79.
26. Cakir B., Schmidt R., Reichel H., Kafer W. Lumbar disk herniation: what are reliable criterions indicative for surgery?. Orthopedics 2009, 32:589.
27. Carl A., Ledet E., Yuan H., Sharan A. New developments in nucleus pulposus replacement technology. Spine J 2004, 4:S325-S329.
28. Cassidy J.D., Côté P., Carroll L.J., Kristman V. Incidence and course of low back pain episodes in the general population. Spine 2005, 30:2817-2823.
29. Cassinelli E.H., Hall R.A., Kang J.D. Biochemistry of intervertebral disc degeneration and the potential for gene therapy applications. Spine J 2001, 1:205-214.
30. Chan W.C., Sze K.L., Samartzis D., Leung V.Y., Chan D. Structure and biology of the intervertebral disk in health and disease. Orthop Clin North Am 2011, 42:447-464.
31. Chang G., Kim H.J., Kaplan D., Vunjak-Novakovic G., Kandel R. Porous silk scaffolds can be used for tissue engineering annulus fibrosus. Eur Spine J 2007, 16:1848-1857.
32. Cheng Y.-H., Yang S.-H., Yang K.-C., Chen M.-P., Lin F.-H. The effects of ferulic acid on nucleus pulposus cells under hydrogen peroxide-induced oxidative stress. Process Biochem 2011, 46:1670-1677.
33. Cheung K.M.C., Al Ghazi S. (i) Current understanding of low back pain and intervertebral disc degeneration: epidemiological perspectives and phenotypes for genetic studies. Curr Orthop 2008, 22:237-244.
34. Chou A.I., Nicoll S.B. Characterization of photocrosslinked alginate hydrogels for nucleus pulposus cell encapsulation. J Biomed Mater Res A 2009, 91A:187-194.
35. Choy D.S. Percutaneous laser disc decompression (PLDD): twelve years' experience with 752 procedures in 518 patients. J Clin Laser Med Surg 1998, 16:325-331.
36. Chung C., Burdick J.A. Engineering cartilage tissue. Adv Drug Deliv Rev 2008, 60:243-262.
37. Civriz Bozdag S., Bay M., Ayyildiz E., Topcuoglu P., Ilhan O. Impact of age and diagnosis on viability during centrifugation and cryopreservation of peripheral blood stem cell products. Transfus Apher Sci 2012, 47:117-120.
38. Clouet J., Vinatier C., Merceron C., Pot-Vaucel M., Hamel O., Weiss P., et al. The intervertebral disc: from pathophysiology to tissue engineering. Joint Bone Spine 2009, 76:614-618.
39. Colombini A., Lombardi G., Corsi M.M., Banfi G. Pathophysiology of the human intervertebral disc. Int J Biochem Cell Biol 2008, 40:837-842.
40. Coventry M.B., Ghormley R.K., Kernohan J.W. The intervertebral disc: its microscopic anatomy and pathology. Part I. Anatomy, development, and physiology. J Bone Joint Surg Am 1945, 27:105-112.
41. Dang J.M., Sun D.D.N., Shin-Ya Y., Sieber A.N., Kostuik J.P., Leong K.W. Temperature-responsive hydroxybutyl chitosan for the culture of mesenchymal stem cells and intervertebral disk cells. Biomaterials 2006, 27:406-418.
42. Denaro L., Longo U.G., Denaro V. Vertebroplasty and kyphoplasty: reasons for concern?. Orthop Clin North Am 2009, 40:465-471.
43. DePalma M.J., Ketchum J.M., Saullo T.R. Multivariable analyses of the relationships between age, gender, and body mass index and the source of chronic low back pain. Pain Med 2012, 13:498-506.
44. Deyo R., Ching A., Matsen L., Martin B., Kreuter W., Jarvik J., et al. Use of bone morphogenetic proteins in spinal fusion surgery for older adults with lumbar stenosis: trends, complications, repeat surgery, and charges. Spine (Phila Pa 1976) 2012, 37:222-230.
45. Di Martino A., Vaccaro A.R., Lee J.Y., Denaro V., Lim M.R. Nucleus pulposus replacement: basic science and indications for clinical use. Spine 2005, 30:S16-S22.
46. Dickerman R., Reynolds A., Morgan B. Polyetheretherketone (PEEK) cage filled with bone morphogenic protein and demineralised bone matrix in anterior cervical discectomy and fusion. Int Orthop 2008, 32:717.
47. Don A.S., Carragee E. A brief overview of evidence-informed management of chronic low back pain with surgery. Spine J 2008, 8:258-265.
48. Dusseault J., Tam S.K., Ménard M., Polizu S., Jourdan G., Yahia L.H., et al. Evaluation of alginate purification methods: effect on polyphenol, endotoxin, and protein contamination. J Biomed Mater Res A 2006, 76A:243-251.
49. Freemont A.J., Peacock T.E., Goupille P., Hoyland J.A., O'Brien J., Jayson M.I.V. Nerve ingrowth into diseased intervertebral disc in chronic back pain. Lancet 1997, 350:178-181.
50. Freemont A.J., Watkins A., Le Maitre C., Baird P., Jeziorska M., Knight M.T.N., et al. Nerve growth factor expression and innervation of the painful intervertebral disc. J Pathol 2002, 197:286-292.
51. Freimark D., Czermak P. Cell-based regeneration of intervertebral disc defects: review and concepts. Int J Artif Organs 2009, 32:197-203.
52. Fujita N., Miyamoto T., Imai J.-i., Hosogane N., Suzuki T., Yagi M., et al. CD24 is expressed specifically in the nucleus pulposus of intervertebral discs. Biochem Biophys Res Commun 2005, 338:1890-1896.
53. Fukui S., Nitta K., Iwashita N., Tomie H., Nosaka S., Rohof O. Results of intradiscal pulsed radiofrequency for lumbar discogenic pain: comparison with intradiscal electrothermal therapy. Korean J Pain 2012, 25:155-160.
54. Gan J.C., Ducheyne P., Vresilovic E., Shapiro I.M. Bioactive glass serves as a substrate for maintenance of phenotype of nucleus pulposus cells of the intervertebral disc. J Biomed Mater Res 2000, 51:596-604.
55. Ganju A. Isthmic spondylolisthesis. Neurosurg Focus 2002, 13:1-6.
56. Gantenbein-Ritter B., Chan S.W. The evolutionary importance of cell ratio between notochordal and nucleus pulposus cells: an experimental 3-D co-culture study. Eur Spine J 2012, 21:819-825.
57. Gloria A., Borzacchiello A., Causa F., Ambrosio L. Rheological characterization of hyaluronic acid derivatives as injectable materials toward nucleus pulposus regeneration. J Biomater Appl 2012, 26:745-759.
58. Gloria A., Causa F., Santis R., Netti P., Ambrosio L. Dynamic-mechanical properties of a novel composite intervertebral disc prosthesis. J Mater Sci Mater Med 2007, 18:2159-2165.
59. Gloria A., De Santis R., Ambrosio L., Causa F., Tanner K.E. A multi-component fiber-reinforced PHEMA-based hydrogel/HAPEXTM device for customized intervertebral disc prosthesis. J Biomater Appl 2011, 25:795-810.
60. Gloria A., Manto L., De Santis R., Ambrosio L. Biomechanical behavior of a novel composite intervertebral body fusion device. J Appl Biomater Biomech 2008, 6:163-169.
61. Gruber H.E., Ingram J.A., Norton H.J., Hanley E.N.J. Senescence in cells of the aging and degenerating intervertebral disc: immunolocalization of senescence-associated beta-galactosidase in human and sand rat discs. Spine 2007, 32:321-327.
62. Grunhagen T., Wilde G., Soukane D.M., Shirazi-Adl S.A., Urban J.P.G. Nutrient supply and intervertebral disc metabolism. J Bone Joint Surg Am 2006, 88:30-35.
63. Hegewald A.A., Endres M., Abbushi A., Cabraja M., Woiciechowsky C., Schmieder K., et al. Adequacy of herniated disc tissue as a cell source for nucleus pulposus regeneration. J Neurosurg Spine 2011, 14:273-280.
64. Helm S., Deer T.R., Manchikanti L., Datta S., Chopra P., Singh V., et al. Effectiveness of thermal annular procedures in treating discogenic low back pain. Pain Physician 2012, 15:E279-E304.
65. Henriksson H.B., Svanvik T., Jonsson M., Hagman M., Horn M., Lindahl A., et al. Transplantation of human mesenchymal stems cells into intervertebral discs in a xenogeneic porcine model. Spine 2009, 34:141-148.
66. Henriksson H.B., Thornemo M., Karlsson C., Hägg O., Junevik K., Lindahl A., et al. Identification of cell proliferation zones, progenitor cells and a potential stem cell niche in the intervertebral disc region: a study in four species. Spine 2009, 34:2278-2287.
67. Heuer F., Ulrich S., Claes L., Wilke H.-J. Biomechanical evaluation of conventional anulus fibrosus closure methods required for nucleus replacement. J Neurosurg Spine 2008, 9:307-313.
68. Hijikata S.A. A method of percutaneous nuclear extraction. J Toden Hosp 1975, 5:39.
69. Huang X., Zhang X., Wang X., Wang C., Tang B. Microenvironment of alginate-based microcapsules for cell culture and tissue engineering. J Biosci Bioeng 2012, 114:1-8.
70. Iatridis J.C., Hecht A.C. Commentary: Does needle injection cause disc degeneration? News in the continuing debate regarding pathophysiology associated with intradiscal injections. Spine J 2012, 12:336-338.
71. Iatridis J.C., Maclean J.J., Roughley P.J., Alini M. Effects of mechanical loading on intervertebral disc metabolism in vivo. J Bone Joint Surg Am 2006, 88:41-46.
72. Iatridis J.C., Setton L.A., Weidenbaum M., Mow V.C. Alterations in the mechanical behavior of the human lumbar nucleus pulposus with degeneration and aging. J Orthop Res 1997, 15:318-322.
73. Iatridis J.C., Setton L.A., Weidenbaum M., Mow V.C. The viscoelastic behavior of the non-degenerate human lumbar nucleus pulposus in shear. J Biomech 1997, 30:1005-1013.
74. Illien-Jünger S., Pattappa G., Peroglio M., Benneker L.M., Stoddart M.J., Sakai D., et al. Homing of mesenchymal stem cells in induced degenerative intervertebral discs in a whole organ culture system. Spine 2012, 37:1865-1873.
75. Jaikumar S., Kim D.H., Kam A.C. History of minimally invasive spine surgery. Neurosurgery 2002, 51:S1-S14.
76. Jeon O., Bouhadir K.H., Mansour J.M., Alsberg E. Photocrosslinked alginate hydrogels with tunable biodegradation rates and mechanical properties. Biomaterials 2009, 30:2724-2734.
77. Kalb S., Martirosyan N.L., Kalani M.Y.S., Broc G.G., Theodore N. Genetics of the degenerated intervertebral disc. World Neurosurg 2012, 77:491-501.
78. Kalson N.S., Richardson S., Hoyland J.A. Strategies for regeneration of the intervertebral disc. Regen Med 2008, 3:717-729.
79. Katz J.N. Lumbar disc disorders and low-back pain: socioeconomic factors and consequences. J Bone Joint Surg Am 2006, 88:21-24.
80. Kawaguchi Y., Ishihara H., Kanamori M., Yasuda T., Abe Y., Nogami S., et al. Adjacent segment disease following expansive lumbar laminoplasty. Spine J 2007, 7:273-279.
81. Kim K.-W., Ha K.-Y., Lee J.-S., Nam S.-W., Woo Y.-K., Lim T.-H., et al. Notochordal cells stimulate migration of cartilage end plate chondrocytes of the intervertebral disc in in vitro cell migration assays. Spine J 2009, 9:323-329.
82. Kim Y.S., Chin D.K., Yoon D.H., Jin B.H., Cho Y.E. Predictors of successful outcome for lumbar chemonucleolysis: analysis of 3000 cases during the past 14years. Neurosurgery 2002, 51:S123-S128.
83. Kock L., van Donkelaar C., Ito K. Tissue engineering of functional articular cartilage: the current status. Cell Tissue Res 2012, 347:613-627.
84. Kumar N., Wijerathne S.I., Lim W.W., Barry T.W., Nath C., Liang S. Resistive straight leg raise test, resistive forward bend test and heel compression test: novel techniques in identifying secondary gain motives in low back pain cases. Eur Spine J 2012, 21:2280-2286.
85. Kuo C.K., Ma P.X. Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: part 1. Structure, gelation rate and mechanical properties. Biomaterials 2001, 22:511-521.
86. Leahy J.C., Hukins D.W.L. Viscoelastic properties of the nucleus pulposus of the intervertebral disk in compression. J Mater Sci Mater Med 2001, 12:689-692.
87. Lee J.-H., Jung T.-G., Kim H.-S., Jang J.-S., Lee S.-H. Analysis of the incidence and clinical effect of the heterotopic ossification in a single-level cervical artificial disc replacement. Spine J 2010, 10:676-682.
88. Lee J.M., Song J.Y., Baek M., Jung H.-Y., Kang H., Han I.B., et al. Interleukin-1β induces angiogenesis and innervation in human intervertebral disc degeneration. J Orthop Res 2011, 29:265-269.
89. Lemcke J., Al-Zain F., Mutze S., Meier U. Minimally invasive spinal surgery using nucleoplasty and the Dekompressor tool: a comparison of two methods in a one year follow-up. Minim Invasive Neurosurg 2010, 53:236-242.
90. Liang C.Z., Li H., Tao Y.Q., Zhou X.P., Yang Z.R., Xiao Y.X., et al. Dual delivery for stem cell differentiation using dexamethasone and bFGF in/on polymeric microspheres as a cell carrier for nucleus pulposus regeneration. J Mater Sci Mater Med 2012, 23:1097-1107.
91. Liao J.-C., Niu C.-C., Chen W.-J., Chen L.-H. Polyetheretherketone (PEEK) cage filled with cancellous allograft in anterior cervical discectomy and fusion. Int Orthop 2008, 32:643-648.
92. Liebscher T., Haefeli M., Wuertz K., Nerlich A.G., Boos N. Age-related variation in cell density of human lumbar intervertebral disc. Spine 2011, 36:153-159.
93. Liu L.-T., Huang B., Li C.-Q., Zhuang Y., Wang J., Zhou Y. Characteristics of stem cells derived from the degenerated human intervertebral disc cartilage endplate. PLoS One 2011, 6:e26285.
94. Lotz J.C., Haughton V., Boden S.D., An H.S., Kang J.D., Masuda K., et al. New treatments and imaging strategies in degenerative disease of the intervertebral disks. Radiology 2012, 264:6-19.
95. Lubbers T., Abuamona R., Elsharkawy A.E. Percutaneous endoscopic treatment of foraminal and extraforaminal disc herniation at the L5-S1 level. Acta Neurochir (Wien) 2012, 154:1789-1795.
96. Luo X., Pietrobon R., X Sun S., Liu G.G., Hey L. Estimates and patterns of direct health care expenditures among individuals with back pain in the United States. Spine 2004, 29:79-86.
97. Magalhaes F.N., Dotta L., Sasse A., Teixera M.J., Fonoff E.T. Ozone therapy as a treatment for low back pain secondary to herniated disc: a systematic review and meta-analysis of randomized controlled trials. Pain Physician 2012, 15:E115-E129.
98. Mano J.F., Silva G.A., Azevedo H.S., Malafaya P.B., Sousa R.A., Silva S.S., et al. Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends. J R Soc Interface 2007, 4:999-1030.
99. Maroon J.C. Current concepts in minimally invasive discectomy. Neurosurgery 2002, 51:S137-S145.
100. Masuda K., An H.S. Growth factors and the intervertebral disc. Spine J 2004, 4:S330-S340.
101. Masuda K., Aota Y., Muehleman C., Imai Y., Okuma M., Thonar E.J., et al. A novel rabbit model of mild, reproducible disc degeneration by an anulus needle puncture: correlation between the degree of disc injury and radiological and histological appearances of disc degeneration. Spine (Phila Pa 1976) 2005, 30:5-14.
102. Masuda K., Lotz J.C. New challenges for intervertebral disc treatment using regenerative medicine. Tissue Eng Part B Rev 2010, 16:147-158.
103. Matsumoto T., Cooper G.M., Gharaibeh B., Meszaros L.B., Li G., Usas A., et al. Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of muscle-derived stem cells expressing bone morphogenetic protein 4 and soluble flt-1. Arthritis Rheum 2009, 60:1390-1405.
104. McAfee P.C. The indications for lumbar and cervical disc replacement. Spine J 2004, 4:S177-S181.
105. Meikle S.T., Perugini V., Guildford A.L., Santin M. Synthesis, characterisation and in vitro anti-angiogenic potential of dendron VEGF blockers. Macromol Biosci 2011, 11:1761-1765.
106. Meisel H.J., Siodla V., Ganey T., Minkus Y., Hutton W.C., Alasevic O.J. Clinical experience in cell-based therapeutics: disc chondrocyte transplantation: a treatment for degenerated or damaged intervertebral disc. Biomol Eng 2007, 24:5-21.
107. Ménard M., Dusseault J., Langlois G., Baille W.E., Tam S.K., Yahia L., et al. Role of protein contaminants in the immunogenicity of alginates. J Biomed Mater Res B Appl Biomater 2010, 93B:333-340.
108. Meyerrose T., Olson S., Pontow S., Kalomoiris S., Jung Y., Annett G., et al. Mesenchymal stem cells for the sustained in vivo delivery of bioactive factors. Adv Drug Deliv Rev 2010, 62:1167-1174.
109. Meyers K., Tauber M., Sudin Y., Fleischer S., Arnin U., Girardi F., et al. Use of instrumented pedicle screws to evaluate load sharing in posterior dynamic stabilization systems. Spine J 2008, 8:926-932.
110. Minogue B., Richardson S., Zeef L., Freemont A., Hoyland J. Transcriptional profiling of bovine intervertebral disc cells: implications for identification of normal and degenerate human intervertebral disc cell phenotypes. Arthritis Res Ther 2010, 12:R22.
111. Minogue B.M., Richardson S.M., Zeef L.A.H., Freemont A.J., Hoyland J.A. Characterization of the human nucleus pulposus cell phenotype and evaluation of novel marker gene expression to define adult stem cell differentiation. Arthritis Rheum 2010, 62:3695-3705.
112. Misteli H., Wolff T., Füglistaler P., Gianni-Barrera R., Gürke L., Heberer M., et al. High-throughput flow cytometry purification of transduced progenitors expressing defined levels of vascular endothelial growth factor induces controlled angiogenesis in vivo. Stem Cells 2010, 28:611-619.
113. Miyamoto K., Masuda K., Kim J.G., Inoue N., Akeda K., Andersson G.B.J., et al. Intradiscal injections of osteogenic protein-1 restore the viscoelastic properties of degenerated intervertebral discs. Spine J 2006, 6:692-703.
114. Moore R. The vertebral endplate: disc degeneration, disc regeneration. Eur Spine J 2006, 15:333-337.
115. Murrell W., Sanford E., Anderberg L., Cavanagh B., Mackay-Sim A. Olfactory stem cells can be induced to express chondrogenic phenotype in a rat intervertebral disc injury model. Spine J 2009, 9:585-594.
116. Nerurkar N.L., Baker B.M., Sen S., Wible E.E., Elliott D.M., Mauck R.L. Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus. Nat Mater 2009, 8:986-992.
117. Nerurkar N.L., Elliott D.M., Mauck R.L. Mechanical design criteria for intervertebral disc tissue engineering. J Biomech 2010, 43:1017-1030.
118. O'Sullivan P. Diagnosis and classification of chronic low back pain disorders: maladaptive movement and motor control impairments as underlying mechanism. Man Ther 2005, 10:242-255.
119. Oliveira J.T., Gardel L.S., Rada T., Martins L., Gomes M.E., Reis R.L. Injectable gellan gum hydrogels with autologous cells for the treatment of rabbit articular cartilage defects. J Orthop Res 2010, 28:1193-1199.
120. Oliveira J.T., Martins L., Picciochi R., Malafaya P.B., Sousa R.A., Neves N.M., et al. Gellan gum: a new biomaterial for cartilage tissue engineering applications. J Biomed Mater Res A 2010, 93A:852-863.
121. Oliveira J.T., Santos T.C., Martins L., Picciochi R., Marques A.P., Castro A.G., et al. Gellan gum injectable hydrogels for cartilage tissue engineering applications: in vitro studies and preliminary in vivo evaluation. Tissue Eng Part A 2010, 16:343-353.
122. Oliveira J.T., Santos T.C., Martins L., Silva M.A., Marques A.P., Castro A.G., et al. Performance of new gellan gum hydrogels combined with human articular chondrocytes for cartilage regeneration when subcutaneously implanted in nude mice. J Tissue Eng Regen Med 2009, 3:493-500.
123. Onik G., Helms C.A., Ginsberg L., Hoaglund F.T., Morris J. Percutaneous lumbar diskectomy using a new aspiration probe: porcine and cadaver model. Radiology 1985, 155:251-252.
124. Orive G., Tam S.K., Pedraz J.L., Hallé J.-P. Biocompatibility of alginate-poly-l-lysine microcapsules for cell therapy. Biomaterials 2006, 27:3691-3700.
125. Ozgur B.M., Yoo K., Rodriguez G., Taylor W.R. Minimally-invasive technique for transforaminal lumbar interbody fusion (TLIF). Eur Spine J 2005, 14:887-894.
126. Parr A.T., Diwan S., Abdi S. Lumbar interlaminar epidural injections in managing chronic low back and lower extremity pain: a systematic review. Pain Physician 2009, 12:163-188.
127. Pereira D.R., Silva-Correia J., Caridade S.G., Oliveira J.T., Sousa R.A., Salgado A.J., et al. Development of gellan gum-based microparticles/hydrogel matrices for application in the intervertebral disc regeneration. Tissue Eng Part C Methods 2011, 17:961-972.
128. Pereira D.R., Silva-Correia J., Oliveira J.M., Reis R.L. Hydrogels in acellular and cellular strategies for intervertebral disc regeneration. J Tissue Eng Regen Med 2013, 7:85-98.
129. Peroglio M., Grad S., Mortisen D., Sprecher C., Illien-Jünger S., Alini M., et al. Injectable thermoreversible hyaluronan-based hydrogels for nucleus pulposus cell encapsulation. Eur Spine J 2012, 21:839-849.
130. Raj P.P. Intervertebral disc: anatomy-physiology-pathophysiology-treatment. Pain Pract 2008, 8:18-44.
131. Rajpurohit R., Risbud M., Ducheyne P., Vresilovic E., Shapiro I. Phenotypic characteristics of the nucleus pulposus: expression of hypoxia inducing factor-1, glucose transporter-1 and MMP-2. Cell Tissue Res 2002, 308:401-407.
132. Reitmaier S., Wolfram U., Ignatius A., Wilke H.-J., Gloria A., Martín-Martínez J.M., et al. Hydrogels for nucleus replacement - facing the biomechanical challenge. J Mech Behav Biomed Mater 2012, 14:67-77.
133. Revell P., Damien E., Di Silvio L., Gurav N., Longinotti C., Ambrosio L. Tissue engineered intervertebral disc repair in the pig using injectable polymers. J Mater Sci Mater Med 2007, 18:303-308.
134. Reza A.T., Nicoll S.B. Characterization of novel photocrosslinked carboxymethylcellulose hydrogels for encapsulation of nucleus pulposus cells. Acta Biomater 2010, 6:179-186.
135. Ribatti D., Nico B., Vacca A., Presta M. The gelatin sponge-chorioallantoic membrane assay. Nat Protoc 2006, 1:85-91.
136. Richardson S.M., Mobasheri A., Freemont A.J., Hoyland J.A. Intervertebral disc biology, degeneration and novel tissue engineering and regenerative medicine therapies. Histol Histopathol 2007, 22:1033-1041.
137. Risbud M.V., Guttapalli A., Tsai T.-T., Lee J.Y., Danielson K.G., Vaccaro A.R., et al. Evidence for skeletal progenitor cells in the degenerate human intervertebral disc. Spine 2007, 32:2537-2544.
138. Roberts S., Caterson B., Menage J., Evans E.H., Jaffray D.C., Eisenstein S.M. Matrix metalloproteinases and aggrecanase: their role in disorders of the human intervertebral disc. Spine (Phila Pa 1976) 2000, 25:3005-3013.
139. Roberts S., Eisenstein S.M., Menage J., Evans E.H., Ashton I.K. Mechanoreceptors in intervertebral discs: morphology, distribution, and neuropeptides. Spine 1995, 20:2645-2651.
140. Roberts S., Evans H., Trivedi J., Menage J. Histology and pathology of the human intervertebral disc. J Bone Joint Surg Am 2006, 88:10-14.
141. Roughley P., Hoemann C., DesRosiers E., Mwale F., Antoniou J., Alini M. The potential of chitosan-based gels containing intervertebral disc cells for nucleus pulposus supplementation. Biomaterials 2006, 27:388-396.
142. Rutges J., Creemers L.B., Dhert W., Milz S., Sakai D., Mochida J., et al. Variations in gene and protein expression in human nucleus pulposus in comparison with annulus fibrosus and cartilage cells: potential associations with aging and degeneration. Osteoarthritis Cartilage 2010, 18:416-423.
143. Rutges J.P.H.J., Duit R.A., Kummer J.A., Oner F.C., van Rijen M.H., Verbout A.J., et al. Hypertrophic differentiation and calcification during intervertebral disc degeneration. Osteoarthritis Cartilage 2010, 18:1487-1495.
144. Saal J.S., Saal J.A. Management of chronic discogenic low back pain with a thermal intradiscal catheter. A preliminary report. Spine (Phila Pa 1976) 2000, 25:382-388.
145. Sah R.L., Ratcliffe A. Translational models for musculoskeletal tissue engineering and regenerative medicine. Tissue Eng Part B Rev 2010, 16:1-3.
146. Sato M., Kikuchi M., Ishihara M., Asazuma T., Kikuchi T., Masuoka K., et al. Tissue engineering of the intervertebral disc with cultured annulus fibrosus cells using atelocollagen honeycombshaped scaffold with a membrane seal (ACHMS scaffold). Med Biol Eng Comput 2003, 41:365-371.
147. Schek R.M., Michalek A.J., Iatridis J.C. Genipin-crosslinked fibrin hydrogels as a potential adhesive to augment intervertebral disc annulus repair. Eur Cell Mater 2011, 21:373-383.
148. Schimizzi A.L., Massie J.B., Murphy M., Perry A., Kim C.W., Garfin S.R., et al. High-molecular-weight hyaluronan inhibits macrophage proliferation and cytokine release in the early wound of a preclinical postlaminectomy rat model. Spine J 2006, 6:550-556.
149. Schimmel J.J., Poeschmann M.S., Horsting P.P., Schonfeld D.H., van Limbeek J., Pavlov P.W. PEEK cages in lumbar fusion: mid-term clinical outcome and radiological fusion. J Spinal Disord Tech 2012, [ahead of print]. 10.1097/BSD.0b013e31826eaf74.
150. Scholz B., Kinzelmann C., Benz K., Mollenhauer J., Wurst H., Schlosshauer B. Suppression of adverse angiogenesis in an albumin-based hydrogel for articular cartilage and intervertebral disc regeneration. Eur Cell Mater 2010, 20:24-37.
151. Séguin C.A., Grynpas M.D., Pilliar R.M., Waldman S.D., Kandel R.A. Tissue engineered nucleus pulposus tissue formed on a porous calcium polyphosphate substrate. Spine 2004, 29:1299-1306.
152. Shankar H., Scarlett J.A., Abram S.E. Anatomy and pathophysiology of intervertebral disc disease. Tech Reg Anesth Pain Manage 2009, 13:67-75.
153. Silva-Correia J., Gloria A., Oliveira M.B., Mano J.F., Oliveira J.M., Ambrosio L., et al. Rheological and mechanical properties of acellular and cell-laden methacrylated gellan gum hydrogels. J Biomed Mater Res A 2013, 10.1002/jbm.a.34650.
154. Silva-Correia J., Miranda-Gonçalves V., Salgado A.J., Sousa N., Oliveira J.M., Reis R.M., et al. Angiogenic potential of gellan gum-based hydrogels for application in nucleus pulposus regeneration: in vivo study. Tissue Eng Part A 2012, 18:1203-1212.
155. Silva-Correia J., Oliveira J.M., Caridade S.G., Oliveira J.T., Sousa R.A., Mano J.F., et al. Gellan gum-based hydrogels for intervertebral disc tissue-engineering applications. J Tissue Eng Regen Med 2011, 5:e97-e107.
156. Silva-Correia J., Oliveira J.M., Oliveira J.T., Sousa R.A., Reis R.L. Photo-crosslinked gellan gum-based hydrogels: methods and uses thereof 2010, [WO2011/119059, Priority date: 105030 26032010 PT].
157. Silva-Correia J., Zavan B., Vindigni V., Silva T.H., Oliveira J.M., Abatangelo G., et al. Biocompatibility evaluation of ionic- and photo-crosslinked methacrylated gellan gum hydrogels: in vitro and in vivo study. Adv Healthc Mater 2013, 2:568-575.
158. Smith L., Garvin P.J., Gesler R.M., Jennings R.B. Enzyme dissolution of the nucleus pulposus. Nature 1963, 198:1311-1312.
159. Smith L.J., Nerurkar N.L., Choi K.-S., Harfe B.D., Elliott D.M. Degeneration and regeneration of the intervertebral disc: lessons from development. Dis Model Mech 2011, 4:31-41.
160. Sowa G., Vadalà G., Studer R., Kompel J., Iucu C., Georgescu H., et al. Characterization of intervertebral disc aging: longitudinal analysis of a rabbit model by magnetic resonance imaging, histology, and gene expression. Spine 2008, 33:1821-1828.
161. Su W.-Y., Chen Y.-C., Lin F.-H. Injectable oxidized hyaluronic acid/adipic acid dihydrazide hydrogel for nucleus pulposus regeneration. Acta Biomater 2010, 6:3044-3055.
162. Suh J.-K.F., Matthew H.W.T. Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: a review. Biomaterials 2000, 21:2589-2598.
163. Swan J., Hurwitz E., Malek F., van den Haak E., Cheng I., Alamin T., et al. Surgical treatment for unstable low-grade isthmic spondylolisthesis in adults: a prospective controlled study of posterior instrumented fusion compared with combined anterior-posterior fusion. Spine J 2006, 6:606-614.
164. Tam S.K., Dusseault J., Polizu S., Ménard M., Hallé J.-P., Yahia L.H. Impact of residual contamination on the biofunctional properties of purified alginates used for cell encapsulation. Biomaterials 2006, 27:1296-1305.
165. Tang S., Rebholz B.J. Does lumbar microdiscectomy affect adjacent segmental disc degeneration? A finite element study. J Surg Res 2013, 182:62-67.
166. Thomas J.D., Fussell G., Sarkar S., Lowman A.M., Marcolongo M. Synthesis and recovery characteristics of branched and grafted PNIPAAm-PEG hydrogels for the development of an injectable load-bearing nucleus pulposus replacement. Acta Biomater 2010, 6:1319-1328.
167. Thongtrangan I., Le H., Park J., Kim D.H. Minimally invasive spinal surgery: a historical perspective. Neurosurg Focus 2004, 16:E13.
168. Turgut M., Uslu S., Uysal A., Yurtseven M., Üstün H. Changes in vascularity of cartilage endplate of degenerated intervertebral discs in response to melatonin administration in rats. Neurosurg Rev 2003, 26:133-138.
169. Urban J., Roberts S. Degeneration of the intervertebral disc. Arthritis Res Ther 2003, 5:120-130.
170. Urban J.P.G., McMullin J.F. Swelling pressure of the lumbar intervertebral discs: influence of age, spinal level, composition, and degeneration. Spine 1988, 13:179-187.
171. Urban J.P.G., Roberts S., Ralphs J.R. The nucleus of the intervertebral disc from development to degeneration. Am Zool 2000, 40:53-61.
172. Urban J.P.G., Winlove C.P. Pathophysiology of the intervertebral disc and the challenges for MRI. J Magn Reson Imaging 2007, 25:419-432.
173. Vadalà G., Denaro E., Sobajima S., Kang J.D., Gilbertson L.G. Stem cell therapy for intervertebral disc degeneration: in vitro study. J Bone Joint Surg Br 2005, 87-B:204-205.
174. Vadalà G., Mozetic P., Rainer A., Centola M., Loppini M., Trombetta M., et al. Bioactive electrospun scaffold for annulus fibrosus repair and regeneration. Eur Spine J 2012, 21:20-26.
175. Vadalà G., Russo F., Patappa G., Schiuma D., Peroglio M., Benneker L.M., et al. The transpedicular approach as an alternative route for intervertebral disc regeneration. Spine 2013, 38:E319-E324.
176. Van den Velden J., De Bakker D.H., Claessens A.A.M.C., Schellevis F.G. A national study of illness encountered in general practitioners' surgeries. Basic report: morbidity in general practice 1991, NIVEL, Utrecht.
177. Van Hoof W., Volkaerts K., O'Sullivan K., Verschueren S., Dankaerts W. Comparing lower lumbar kinematics in cyclists with low back pain (flexion pattern) versus asymptomatic controls-field study using a wireless posture monitoring system. Man Ther 2012, 17:312-317.
178. Vonk L.A., Kroeze R.J., Doulabi B.Z., Hoogendoorn R.J., Huang C., Helder M.N., et al. Caprine articular, meniscus and intervertebral disc cartilage: an integral analysis of collagen network and chondrocytes. Matrix Biol 2010, 29:209-218.
179. Weiler C., Nerlich A., Schaaf R., Bachmeier B., Wuertz K., Boos N. Immunohistochemical identification of notochordal markers in cells in the aging human lumbar intervertebral disc. Eur Spine J 2010, 19:1761-1770.
180. Widanarko B., Legg S., Stevenson M., Devereux J., Eng A., Mannetje A., et al. Gender differences in work-related risk factors associated with low back symptoms. Ergonomics 2012, 55:327-342.
181. Wilke H.-J., Neef P., Hinz B., Seidel H., Claes L. Intradiscal pressure together with anthropometric data - a data set for the validation of models. Clin Biomech 2001, 16(Supplement 1):S111-S126.
182. Woods B.I., Sowa G., Vo N., Kang J.D. A change in strategy: the use of regenerative medicine and tissue engineering to augment the course of intervertebral disc degeneration. Oper Tech Orthop 2010, 20:144-153.
183. Woolf A.D., Pfleger B. Burden of major musculoskeletal conditions. Bull World Health Organ 2003, 81:646-656.
184. Xu H., Tang H., Guan X., Jiang F., Xu N., Ju W., et al. Biomechanical comparison of posterior lumbar interbody fusion and transforaminal lumbar interbody fusion by finite element analysis. Neurosurgery 2013, 72:21-26.
185. Yang S.-H., Chen P.-Q., Chen Y.-F., Lin F.-H. An in-vitro study on regeneration of human nucleus pulposus by using gelatin/chondroitin-6-sulfate/hyaluronan tri-copolymer scaffold. Artif Organs 2005, 29:806-814.
186. Zhang H.Q., Lin M.Z., Ge L., Li J.S., Wu J.H., Liu J.Y. Surgical management by one-stage posterior transforaminal lumbar debridement, interbody fusion, and posterior instrumentation for lumbo-sacral tuberculosis in the aged. Arch Orthop Trauma Surg 2012, 132:1677-1683.
187. Zhao C.-Q., Wang L.-M., Jiang L.-S., Dai L.-Y. The cell biology of intervertebral disc aging and degeneration. Ageing Res Rev 2007, 6:247-261.
188. Zigler J., Delamarter R., Spivak J.M., Linovitz R.J., Danielson GOr, Haider T.T., et al. Results of the prospective, randomized, multicenter Food and Drug Administration investigational device exemption study of the ProDisc-L total disc replacement versus circumferential fusion for the treatment of 1-level degenerative disc disease. Spine (Phila Pa 1976) 2007, 32:1155-1162.