Intervertebral Disk Nutrition: A Review of Factors Influencing Concentrations of Nutrients and Metabolites

Orthopedic Clinics of North America

Volumn 42, Issue 4, 2011, Pages 465-477

  Grunhagen, Thijs ^a,b   Shirazi Adl, Aboulfazl ^c   Fairbank, Jeremy C T ^d   Urban, Jill P G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b PHILIPS RESEARCH LABORATORIES   (Netherlands)

^c ÉCOLE POLYTECHNIQUE DE MONTRÉAL   (Canada)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Calcification; Diffusion; Disk; End plate; Glucose; Intervertebral; Oxygen; PH

Indexed keywords

GLUCOSE; GROWTH DIFFERENTIATION FACTOR 5; OXYGEN; PROTEOGLYCAN;

ARTERIAL CIRCULATION; BIOLOGICAL THERAPY; BONE BLOOD FLOW; BONE CELL; BONE MATRIX; CAPILLARY FLOW; CARTILAGINOUS ENDPLATE; CELL ACTIVITY; CELL METABOLISM; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONTRAST ENHANCEMENT; DIFFUSION; DISEASE ASSOCIATION; HUMAN; HYALINE CARTILAGE; INTERVERTEBRAL DISK; INTERVERTEBRAL DISK DEGENERATION; METABOLITE; MOLECULAR SIZE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUTRIENT CONCENTRATION; NUTRIENT SUPPLY; PERMEABILITY; POROSITY; PRIORITY JOURNAL; REVIEW; SPINE; TRANSPORT AT THE CELLULAR LEVEL;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; ANIMALS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DOGS; EXTRACELLULAR MATRIX; FOOD; GLUCOSE; HOMEOSTASIS; HUMANS; INTERVERTEBRAL DISC; INTERVERTEBRAL DISC DEGENERATION; MIDDLE AGED; OXYGEN CONSUMPTION; RABBITS; RISK FACTORS; SENSITIVITY AND SPECIFICITY;

EID: 80053183939     PISSN: 00305898     EISSN: 15581373     Source Type: Journal    
DOI: 10.1016/j.ocl.2011.07.010     Document Type: Review

References (112)

1. Beadle O.A. The intervertebral discs. Observations on their normal and morbid anatomy in relation to certain spinal deformities 1931, His Majesty's Stationery Office, London.
2. Nerlich A.G., Schaaf R., Walchli B., et al. Temporo-spatial distribution of blood vessels in human lumbar intervertebral discs. Eur Spine J 2007, 16(4):547-555.
3. Brodin H. Paths of nutrition in articular cartilage and intervertebral discs. Acta Orthop Scand 1955, 24:177-183.
4. Ogata K., Whiteside L.A. 1980 Volvo award winner in basic science. Nutritional pathways of the intervertebral disc. An experimental study using hydrogen washout technique. Spine 1981, 6:211-216.
5. Ratcliffe J.F. The arterial anatomy of the developing human dorsal and lumbar vertebral body. A microarteriographic study. J Anat 1981, 133(Pt 4):625-638.
6. Hassler O. The human intervertebral disc. A micro-angiographical study of its vascular supply at various ages. Acta Orthop Scand 1970, 40:765-772.
7. Crock H.V., Yoshizawa H., Kame S.K. Observations on the venous drainage of the human vertebral body. J Bone Joint Surg Br 1973, 55(3):528-533.
8. Crock H.V., Yoshizawa H. The blood supply of the vertebral column. Clin Orthop Relat Res 1976, 115:6-21.
9. Ratcliffe J.F. The arterial anatomy of the adult human lumbar vertebral body: a microarteriographic study. J Anat 1980, 131(1):57-79.
10. Ratcliffe J.F. The anatomy of the fourth and fifth lumbar arteries in humans: an arteriographic study in one hundred live subjects. J Anat 1982, 135:753-761.
11. Crock H.V., Goldwasser M. Anatomic studies of the circulation in the region of the vertebral end-plate in adult greyhound dogs. Spine 1984, 9:702-706.
12. Crock H.V., Goldwasser M., Yoshizawa H. Vascular anatomy related to the intervertebral disc. Biology of the intervertebral disc 1991, 109-133. CRC Press, Boca Raton (FL). P. Ghosh (Ed.).
13. Chandraraj S., Briggs C.A., Opeskin K. Disc herniations in the young and end-plate vascularity. Clin Anat 1998, 11(3):171-176.
14. Kobayashi S., Baba H., Takeno K., et al. Fine structure of cartilage canal and vascular buds in the rabbit vertebral endplate. Laboratory investigation. J Neurosurg Spine 2008, 9(1):96-103.
15. Oki S., Matsuda Y., Itoh T., et al. Scanning electron microscopic observations of the vascular structure of vertebral end-plates in rabbits. J Orthop Res 1994, 12(3):447-449.
16. Moore R.J. The vertebral end-plate: what do we know?. Eur Spine J 2000, 9(2):92-96.
17. Roberts S., Menage J., Urban J.P. Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine 1989, 14:166-174.
18. Brown M.F., Hukkanen M.V., McCarthy I.D., et al. Sensory and sympathetic innervation of the vertebral endplate in patients with degenerative disc disease. J Bone Joint Surg Br 1997, 79(1):147-153.
19. Wallace A.L., Wyatt B.C., McCarthy I.D., et al. Humoral regulation of blood flow in the vertebral endplate. Spine 1994, 19(12):1324-1328.
20. Holm S., Nachemson A. Nutrition of the intervertebral disc: acute effects of cigarette smoking. An experimental animal study. Ups J Med Sci 1988, 93(1):91-99.
21. Uematsu Y., Matuzaki H., Iwahashi M. Effects of nicotine on the intervertebral disc: an experimental study in rabbits. J Orthop Sci 2001, 6(2):177-182.
22. Iwahashi M., Matsuzaki H., Tokuhashi Y., et al. Mechanism of intervertebral disc degeneration caused by nicotine in rabbits to explicate intervertebral disc disorders caused by smoking. Spine 2002, 27(13):1396-1401.
23. Amonoo-Kuofi H.S. Morphometric changes in the heights and anteroposterior diameters of the lumbar intervertebral discs with age. J Anat 1991, 175:159-168.
24. Aydinlioglu A., Diyarbakirli S., Keles P. Heights of the lumbar intervertebral discs related to age in Turkish individuals. Tohoku J Exp Med 1999, 188(1):11-22.
25. Laffosse J.M., Accadbled F., Molinier F., et al. Correlations between effective permeability and marrow contact channels surface of vertebral endplates. J Orthop Res 2010, 28(9):1229-1234.
26. Urban J.P., Holm S., Maroudas A., et al. Nutrition of the intervertebral disc: effect of fluid flow on solute transport. Clin Orthop 1982, 170:296-302.
27. Katz M.M., Hargens A.R., Garfin S.R. Intervertebral disc nutrition. Diffusion versus convection. Clin Orthop 1986, (210):243-245.
28. Ferguson S.J., Ito K., Nolte L.P. Fluid flow and convective transport of solutes within the intervertebral disc. J Biomech 2004, 37(2):213-221.
29. Nachemson A., Elfstrom G. Intravital dynamic pressure measurements in lumbar discs. A study of common movements, maneuvers and exercises. Scand J Rehabil Med 1970, 2(Suppl 1):1-40.
30. Wilke H.J., Neef P., Caimi M., et al. New in vivo measurements of pressures in the intervertebral disc in daily life. Spine 1999, 24(8):755-762.
31. Boos N., Wallin A., Gbedegbegnon T., et al. Quantitative MR imaging of lumbar intervertebral discs and vertebral bodies: influence of diurnal water content variations. Radiology 1993, 188:351-354.
32. Bernick S., Cailliet R. Vertebral end-plate changes with aging of human vertebrae. Spine 1982, 7(2):97-102.
33. Whalen J.L., Parke W.W., Mazur J.M., et al. The intrinsic vasculature of developing vertebral end plates and its nutritive significance to the intervertebral discs. J Pediatr Orthop 1985, 5(4):403-410.
34. Rudert M., Tillmann B. Detection of lymph and blood vessels in the human intervertebral disc by histochemical and immunohistochemical methods. Anat Anz 1993, 175(3):237-242.
35. Roberts S., Urban J.P.G., Evans H., et al. Transport properties of the human cartilage endplate in relation to its composition and calcification. Spine 1996, 21:415-420.
36. Shibuya K. Experimental and clinical studies on metabolism with the intervertebral disc. Nihon Seikeigeka Gakkai Zasshi 1970, 44:1-24.
37. Travascio F., Jackson A.R., Brown M.D., et al. Relationship between solute transport properties and tissue morphology in human annulus fibrosus. J Orthop Res 2009, 27(12):1625-1630.
38. O'Hare D., Winlove C.P., Parker K.H. Electrochemical method for direct measurement of oxygen concentration and diffusivity in the intervertebral disc: electrochemical characterization and tissue-sensor interactions. J Biomed Eng 1991, 13(4):304-312.
39. Jackson A., Gu W. Transport properties of cartilaginous tissues. Curr Rheumatol Rev 2009, 5(1):40-50.
40. Bartels E., Fairbank J.C., Winlove C.P., et al. Measurement of hydrogen and oxygen in isolated intervertebral discs. J Physiol 1995, 483:126.
41. Maroudas A. Transport of solutes through cartilage: permeability to large molecules. J Anat 1976, 122(2):335-347.
42. Grunhagen T. Nutrient transport into intervertebral discs; modelling and electrochemical measurements 2010, [thesis/dissertation], University of Oxford, Oxford (UK).
43. Maroudas A. Biophysical chemistry of cartilaginous tissues with special reference to solute and fluid transport. Biorheology 1975, 12(3-4):233-248.
44. Stairmand J.W., Holm S., Urban J.P. Factors influencing oxygen concentration gradients in the intervertebral disc. A theoretical analysis. Spine (Phila Pa 1976) 1991, 16(4):444-449.
45. de Puky P. The physiological oscillation of the length of the body. Acta Orthop Scand 1935, 6:338-347.
46. Tyrrell A.R., Reilly T., Troup J.D. Circadian variation in stature and the effects of spinal loading. Spine 1985, 10:161-164.
47. Soukane D.M., Shirazi-adl A., Urban J.P. Computation of coupled diffusion of oxygen, glucose and lactic acid in an intervertebral disc. J Biomech 2007, 40(12):2645-2654.
48. Arun R., Freeman B.J., Scammell B.E., et al. 2009 ISSLS Prize Winner: What influence does sustained mechanical load have on diffusion in the human intervertebral disc? an in vivo study using serial postcontrast magnetic resonance imaging. Spine (Phila Pa 1976) 2009, 34(21):2324-2337.
49. Kauppila L.I. Atherosclerosis and disc degeneration/low-back pain-a systematic review. Eur J Vasc Endovasc Surg 2009, 37(6):661-670.
50. Kauppila L.I. Prevalence of stenotic changes in arteries supplying the lumbar spine. A postmortem angiographic study on 140 subjects. Ann Rheum Dis 1997, 56(10):591-595.
51. Kauppila L.I., McAlindon T., Evans S., et al. Disc degeneration/back pain and calcification of the abdominal aorta. A 25-year follow-up study in Framingham. Spine 1997, 22(14):1642-1647.
52. Kurunlahti M., Tervonen O., Vanharanta H., et al. Association of atherosclerosis with low back pain and the degree of disc degeneration. Spine 1999, 24(20):2080-2084.
53. Hangai M., Kaneoka K., Kuno S., et al. Factors associated with lumbar intervertebral disc degeneration in the elderly. Spine J 2008, 8(5):732-740.
54. Leino-Arjas P., Kaila-Kangas L., Solovieva S., et al. Serum lipids and low back pain: an association? A follow-up study of a working population sample. Spine (Phila Pa 1976) 2006, 31(9):1032-1037.
55. Miller J., Schmatz C., Schultz A. Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens. Spine 1988, 13:173-178.
56. Jones J.P., Engleman E.P. Osseous avascular necrosis associated with systemic abnormalities. Arthritis Rheum 1966, 9(5):728-736.
57. Leboeuf-yde C. Smoking and low back pain. A systematic literature review of 41 journal articles reporting 47 epidemiologic studies. Spine (Phila Pa 1976) 1999, 24(14):1463-1470.
58. Goldberg M.S., Scott S.C., Mayo N.E. A review of the association between cigarette smoking and the development of nonspecific back pain and related outcomes. Spine (Phila Pa 1976) 2000, 25(8):995-1014.
59. Hassett G., Hart D.J., Manek N.J., et al. Risk factors for progression of lumbar spine disc degeneration: the Chingford Study. Arthritis Rheum 2003, 48(11):3112-3117.
60. Battie M.C., Videman T., Gill K., et al. 1991 Volvo Award in clinical sciences. Smoking and lumbar intervertebral disc degeneration: an MRI study of identical twins. Spine 1991, 16(9):1015-1021.
61. Hambly M.F., Mooney V. Effect of smoking and pulsed electromagnetic fields on intradiscal pH in rabbits. Spine 1992, 17(Suppl 6):S83-S85.
62. Fogelholm R.R., Alho A.V. Smoking and intervertebral disc degeneration. Med Hypotheses 2001, 56(4):537-539.
63. Nachemson A., Lewin T., Maroudas A., et al. In vitro diffusion of dye through the end-plates and annulus fibrosus of human lumbar intervertebral discs. Acta Orthop Scand 1970, 41:589-607.
64. Pye S.R., Reid D.M., Lunt M., et al. Lumbar disc degeneration: association between osteophytes, end-plate sclerosis and disc space narrowing. Ann Rheum Dis 2007, 66(3):330-333.
65. Muraki S., Yamamoto S., Ishibashi H., et al. Impact of degenerative spinal diseases on bone mineral density of the lumbar spine in elderly women. Osteoporos Int 2004, 15(9):724-728.
66. Rutges J.P., Jagt van der O.P., Oner F.C., et al. Micro-CT quantification of subchondral endplate changes in intervertebral disc degeneration. Osteoarthritis Cartilage 2011, 19(1):89-95.
67. Laffosse J.M., Kinkpe C., Gomez-Brouchet A., et al. Micro-computed tomography study of the subchondral bone of the vertebral endplates in a porcine model: correlations with histomorphometric parameters. Surg Radiol Anat 2010, 32(4):335-341.
68. Weiler C., Nerlich A.G., Zipperer J., et al. 2002 SSE Award Competition in Basic Science: expression of major matrix metalloproteinases is associated with intervertebral disc degradation and resorption. Eur Spine J 2002, 11(4):308-320.
69. Benneker L.M., Heini P.F., Alini M., et al. 2004 Young Investigator Award Winner: vertebral endplate marrow contact channel occlusions and intervertebral disc degeneration. Spine 2005, 30(2):167-173.
70. Vernon-Roberts B. Disc pathology and disease states. The biology of the intervertebral disc 1988, 73-119. CRC press, Boca Raton (FL). P. Ghosh (Ed.).
71. Roberts S., Menage J., Eisenstein S.M. The cartilage end-plate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res 1993, 11(5):747-757.
72. Urban M.R., Fairbank J.C., Etherington P.J., et al. Electrochemical measurement of transport into scoliotic intervertebral discs in vivo using nitrous oxide as a tracer. Spine 2001, 26(8):984-990.
73. Rajasekaran S., Vidyadhara S., Subbiah M., et al. ISSLS prize winner: a study of effects of in vivo mechanical forces on human lumbar discs with scoliotic disc as a biological model: results from serial postcontrast diffusion studies, histopathology and biochemical analysis of twenty-one human lumbar scoliotic discs. Spine (Phila Pa 1976) 2010, 35(21):1930-1943.
74. Bydder G.M. New approaches to magnetic resonance imaging of intervertebral discs, tendons, ligaments, and menisci. Spine 2002, 27(12):1264-1268.
75. Nguyenminh C., Riley L., Ho K.C., et al. Effect of degeneration of the intervertebral disk on the process of diffusion. AJNR Am J Neuroradiol 1997, 18(3):435-442.
76. Rajasekaran S., Naresh-Babu J., Murugan S. Review of postcontrast MRI studies on diffusion of human lumbar discs. J Magn Reson Imaging 2007, 25(2):410-418.
77. Rajasekaran S., Babu J.N., Arun R., et al. ISSLS prize winner: a study of diffusion in human lumbar discs: a serial magnetic resonance imaging study documenting the influence of the endplate on diffusion in normal and degenerate discs. Spine 2004, 29(23):2654-2667.
78. Rajasekaran S., Venkatadass K., Naresh B.J., et al. Pharmacological enhancement of disc diffusion and differentiation of healthy, ageing and degenerated discs: results from in-vivo serial post-contrast MRI studies in 365 human lumbar discs. Eur Spine J 2008, 17(5):626-643.
79. Razaq S., Wilkins R.J., Urban J.P. The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus. Eur Spine J 2003, 12(4):341-349.
80. Ishihara H., Urban J.P. Effects of low oxygen concentrations and metabolic inhibitors on proteoglycan and protein synthesis rates in the intervertebral disc. J Orthop Res 1999, 17(6):829-835.
81. Rinkler C., Heuer F., Pedro M.T., et al. Influence of low glucose supply on the regulation of gene expression by nucleus pulposus cells and their responsiveness to mechanical loading. J Neurosurg Spine 2010, 13(4):535-542.
82. Bibby S.R., Urban J.P. Effect of nutrient deprivation on the viability of intervertebral disc cells. Eur Spine J 2004, 13(8):695-701.
83. Bibby S.R., Fairbank J.C., Urban M.R., et al. Cell viability in scoliotic discs in relation to disc deformity and nutrient levels. Spine 2002, 27(20):2220-2228.
84. Urban J.P., Holm S., Maroudas A. Diffusion of small solutes into the intervertebral disc: as in vivo study. Biorheology 1978, 15(3-4):203-221.
85. Holm S., Maroudas A., Urban J.P., et al. Nutrition of the intervertebral disc: solute transport and metabolism. Connect Tissue Res 1981, 8(2):101-119.
86. Bartels E.M., Fairbank J.C.T., Winlove C.P., et al. Oxygen and lactate concentrations measured in vivo in the intervertebral discs of scoliotic and back pain patients. Spine 1998, 23:1-7.
87. Nachemson A. Intradiscal measurements of pH in patients with lumbar rhizopathies. Acta Orthop Scand 1969, 40:23-42.
88. Kitano T., Zerwekh J.E., Usui Y., et al. Biochemical changes associated with the symptomatic human intervertebral disc. Clin Orthop 1993, (293):372-377.
89. Holm S., Selstam G., Nachemson A. Carbohydrate metabolism and concentration profiles of solutes in the canine lumbar intervertebral disc. Acta Physiol Scand 1982, 115(1):147-156.
90. Maroudas A., Stockwell R.A., Nachemson A., et al. Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. J Anat 1975, 120(1):113-130.
91. Selard E., Shirazi-adl A., Urban J.P. Finite element study of nutrient diffusion in the human intervertebral disc. Spine 2003, 28(17):1945-1953.
92. Bibby S.R., Jones D.A., Ripley R.M., et al. Metabolism of the intervertebral disc: effects of low levels of oxygen, glucose, and pH on rates of energy metabolism of bovine nucleus pulposus cells. Spine 2005, 30(5):487-496.
93. Soukane D.M., Shirazi-adl A., Urban J.P. Analysis of nonlinear coupled diffusion of oxygen and lactic acid in intervertebral discs. J Biomech Eng 2005, 127(7):1121-1126.
94. Soukane D.M., Shirazi-adl A., Urban J.P. Investigation of solute concentrations in a 3D model of intervertebral disc. Eur Spine J 2009, 18(2):254-262.
95. Shirazi-adl A., Taheri M., Urban J.P. Analysis of cell viability in intervertebral disc: effect of endplate permeability on cell population. J Biomech 2010, 43(7):1330-1336.
96. Magnier C., Boiron O., Wendling-Mansuy S., et al. Nutrient distribution and metabolism in the intervertebral disc in the unloaded state: a parametric study. J Biomech 2009, 42(2):100-108.
97. Bron J.L., Helder M.N., Meisel H.J., et al. Repair, regenerative and supportive therapies of the annulus fibrosus: achievements and challenges. Eur Spine J 2009, 18(3):301-313.
98. Kandel R., Roberts S., Urban J.P. Tissue engineering and the intervertebral disc: the challenges. Eur Spine J 2008, 17(Suppl 4):480-491.
99. Kalson N.S., Richardson S., Hoyland J.A. Strategies for regeneration of the intervertebral disc. Regen Med 2008, 3(5):717-729.
100. Masuda K. Biological repair of the degenerated intervertebral disc by the injection of growth factors. Eur Spine J 2008, 17(Suppl 4):441-451.
101. Hubert M.G., Vadala G., Sowa G., et al. Gene therapy for the treatment of degenerative disc disease. J Am Acad Orthop Surg 2008, 16(6):312-319.
102. Le Maitre C.L., Hoyland J.A., Freemont A.J. Interleukin-1 receptor antagonist delivered directly and by gene therapy inhibits matrix degradation in the intact degenerate human intervertebral disc: an in situ zymographic and gene therapy study. Arthritis Res Ther 2007, 9(4):R83.
103. Sakai D. Future perspectives of cell-based therapy for intervertebral disc disease. Eur Spine J 2008, 17(Suppl 4):452-458.
104. Serigano K., Sakai D., Hiyama A., et al. Effect of cell number on mesenchymal stem cell transplantation in a canine disc degeneration model. J Orthop Res 2010, 28(10):1267-1275.
105. Miyamoto K., Masuda K., Kim J.G., et al. Intradiscal injections of osteogenic protein-1 restore the viscoelastic properties of degenerated intervertebral discs. Spine J 2006, 6(6):692-703.
106. Ganey T., Hutton W.C., Moseley T., et al. Intervertebral disc repair using adipose tissue-derived stem and regenerative cells: experiments in a canine model. Spine (Phila Pa 1976) 2009, 34(21):2297-2304.
107. Alini M., Eisenstein S.M., Ito K., et al. Are animal models useful for studying human disc disorders/degeneration?. Eur Spine J 2008, 17(1):2-19.
108. Paesold G., Nerlich A.G., Boos N. Biological treatment strategies for disc degeneration: potentials and shortcomings. Eur Spine J 2007, 16(4):447-468.
109. Hohaus C., Ganey T.M., Minkus Y., et al. Cell transplantation in lumbar spine disc degeneration disease. Eur Spine J 2008, 17(Suppl 4):492-503.
110. A clinical trial to evaluate the safety, tolerability and preliminary effectiveness of single administration intradiscal rhGDF-5 for the treatment of early stage lumbar disc degeneration. Available at: 2011. Accessed August 17, 2011. http://clinicaltrials.gov/ct2/show/NCT01158924.
111. Carragee E.J., Tanner C.M., Khurana S., et al. The rates of false-positive lumbar discography in select patients without low back symptoms. Spine (Phila Pa 1976) 2000, 25(11):1373-1380.
112. Carragee E.J., Don A.S., Hurwitz E.L., et al. 2009 ISSLS Prize Winner: Does discography cause accelerated progression of degeneration changes in the lumbar disc: a ten-year matched cohort study. Spine (Phila Pa 1976) 2009, 34(21):2338-2345.