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Published in: European Spine Journal 9/2014

01-09-2014 | Original Article

The effects of osteoporosis and disc degeneration on vertebral cartilage endplate lesions in rats

Authors: Yin Ding, Jie Jiang, Jian Zhou, Xiuhua Wu, Zhiping Huang, Jianting Chen, Qingan Zhu

Published in: European Spine Journal | Issue 9/2014

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Abstracts

Purpose

Evidence has shown that osteoporosis or intervertebral disc degeneration (IDD) led to cartilage endplate lesions (CEL), but their combined effects on the lesion remain unknown. This study developed an innovative rat model combined ovariectomy (OVX) and cervical muscle section (CMS), and aimed to evaluate the combined effects of osteoporosis and IDD on cartilage endplate lesions of cervical spine.

Methods

Fifty-two Sprague–Dawley female rats were assigned randomly into four groups as follows: the sham group (n = 10) underwent sham surgery; the OVX group (n = 14) was subjected to bilateral ovariectomy; the CMS group (n = 14) had posterior paraspinal muscles cut from C2 to C7; the CMS–OVX group (n = 14) underwent the OVX and CMS surgeries consecutively. Samples of C6–C7 segments were harvested at 12, 18 and 24 weeks post-surgery. Micro-CT analysis was performed to evaluate the CEL, intervertebral disc height (IDH) and structural indices. Histological analysis with Safranine O/fast green stain and histological score were used to observe the characteristics of the degenerative discs.

Results

Ovariectomy surgery resulted in significant changes of most structural indices of the C6 body, such as decrease of percent bone volume and number of bone trabecula at 12 weeks,  and greater changes at 18 and 24 weeks. The CEL following CMS surgery was seen on the ventral, while the CEL in the OVX and sham groups on the peripheral. The CEL was greatest in the CMS–OVX group and significantly greater than that in the CMS and OVX groups at 12 and 18 weeks (P < 0.05). The CMS surgery resulted in significant IDH decrease at 12, 18 and 24 weeks (P < 0.05), while the OVX surgery resulted in mild IDH decrease when compared with the sham group. The IDH in the CMS–OVX group was significantly lower than that in the CMS group at 24 weeks (P < 0.05). Histological evaluation suggested cartilage endplate abrasion at 12 weeks, and in situ calcification at 18 and 24 weeks in the CMS and CMS–OVX groups. Disc degenerative scores were higher following CMS or OVX surgery, and correlated with the CEL and IDH (P < 0.01), respectively.

Conclusions

The present study suggested that a combination of OVX and CMS led to more lesion of cartilage endplate than any one thereof, as well as more decrease of IDH. The lesion and IDH decrease were associated with the disc degeneration levels. The cartilage endplate was worn out at the early stage and calcified in situ later. The results indicate that osteoporosis may deteriorate the disc degeneration at specific time.
Literature
1.
go back to reference Yoshimura N, Muraki S, Oka H, Mabuchi A et al (2009) Prevalence of knee osteoarthritis, lumbar spondylosis, and osteoporosis in Japanese men and women: the research on osteoarthritis/osteoporosis against disability study. J Bone Miner Metab 27(5):620–628PubMedCrossRef Yoshimura N, Muraki S, Oka H, Mabuchi A et al (2009) Prevalence of knee osteoarthritis, lumbar spondylosis, and osteoporosis in Japanese men and women: the research on osteoarthritis/osteoporosis against disability study. J Bone Miner Metab 27(5):620–628PubMedCrossRef
2.
go back to reference Miyakoshi N, Itoi E, Murai H, Wakabayashi I, Ito H, Minato T (2003) Inverse relation between osteoporosis and spondylosis in postmenopausal women as evaluated by bone mineral density and semiquantitative scoring of spinal degeneration. Spine (Phila Pa 1976) 28:492–495 Miyakoshi N, Itoi E, Murai H, Wakabayashi I, Ito H, Minato T (2003) Inverse relation between osteoporosis and spondylosis in postmenopausal women as evaluated by bone mineral density and semiquantitative scoring of spinal degeneration. Spine (Phila Pa 1976) 28:492–495
3.
go back to reference Nanjo Y, Morio Y, Nagashima H et al (2003) Correlation between bone mineral density and intervertebral disk degeneration in pre- and postmenopausal women. J Bone Miner Metab 21(1):22–27PubMedCrossRef Nanjo Y, Morio Y, Nagashima H et al (2003) Correlation between bone mineral density and intervertebral disk degeneration in pre- and postmenopausal women. J Bone Miner Metab 21(1):22–27PubMedCrossRef
4.
go back to reference Margulies JY, Payzer A, Nyska M et al (1996) The relationship between degenerative changes and osteoporosis in the lumbar spine. Clin Orthop Relat Res 324:145–152PubMedCrossRef Margulies JY, Payzer A, Nyska M et al (1996) The relationship between degenerative changes and osteoporosis in the lumbar spine. Clin Orthop Relat Res 324:145–152PubMedCrossRef
5.
go back to reference Zhang Y, Xia J, Qiu Y et al (2012) Correlation between osteoporosis and degeneration of intervertebral discs in aging rats. J Huazhong Univ Sci Technolog Med Sci 32(2):210–215PubMedCrossRef Zhang Y, Xia J, Qiu Y et al (2012) Correlation between osteoporosis and degeneration of intervertebral discs in aging rats. J Huazhong Univ Sci Technolog Med Sci 32(2):210–215PubMedCrossRef
6.
go back to reference Simpson EK, Parkinson IH, Manthey B et al (2001) Intervertebral disc disorganization is related to trabecular bone architecture in the lumbar spine. J Bone Miner Res 16(4):681–687PubMedCrossRef Simpson EK, Parkinson IH, Manthey B et al (2001) Intervertebral disc disorganization is related to trabecular bone architecture in the lumbar spine. J Bone Miner Res 16(4):681–687PubMedCrossRef
7.
go back to reference Wang YX, Griffith JF, Ma HT et al (2011) Relationship between gender, bone mineral density, and disc degeneration in the lumbar spine: a study in elderly subjects using an eight-level MRI-based disc degeneration grading system. Osteoporos Int 22(1):91–96PubMedCrossRef Wang YX, Griffith JF, Ma HT et al (2011) Relationship between gender, bone mineral density, and disc degeneration in the lumbar spine: a study in elderly subjects using an eight-level MRI-based disc degeneration grading system. Osteoporos Int 22(1):91–96PubMedCrossRef
8.
go back to reference Gruber HE, Gordon B, Williams C et al (2003) Bone mineral density of lumbar vertebral end plates in the aging male sand rat spine. Spine 28(16):1766–1772PubMedCrossRef Gruber HE, Gordon B, Williams C et al (2003) Bone mineral density of lumbar vertebral end plates in the aging male sand rat spine. Spine 28(16):1766–1772PubMedCrossRef
9.
go back to reference Wang T, Zhang L, Huang C et al (2004) Relationship between osteopenia and lumbar intervertebral disc degeneration in ovariectomized rats. Calcif Tissue Int 75(3):205–213PubMedCrossRef Wang T, Zhang L, Huang C et al (2004) Relationship between osteopenia and lumbar intervertebral disc degeneration in ovariectomized rats. Calcif Tissue Int 75(3):205–213PubMedCrossRef
10.
go back to reference Luo Y, Zhang L, Wang WY et al (2013) Alendronate retards the progression of lumbar intervertebral disc degeneration in ovariectomized rats. Bone 55(2):439–448PubMedCrossRef Luo Y, Zhang L, Wang WY et al (2013) Alendronate retards the progression of lumbar intervertebral disc degeneration in ovariectomized rats. Bone 55(2):439–448PubMedCrossRef
11.
go back to reference Polikeit A, Nolte LP, Ferguson SJ (2004) Simulated influence of osteoporosis and disc degeneration on the load transfer in a lumbar functional spinal unit. J Biomech 37(7):1061–1069PubMedCrossRef Polikeit A, Nolte LP, Ferguson SJ (2004) Simulated influence of osteoporosis and disc degeneration on the load transfer in a lumbar functional spinal unit. J Biomech 37(7):1061–1069PubMedCrossRef
12.
go back to reference Urban JPG, Smith S, Fairbank JCT (2004) Nutrition of the intervertebral disc. Spine 29(23):2700–2709PubMedCrossRef Urban JPG, Smith S, Fairbank JCT (2004) Nutrition of the intervertebral disc. Spine 29(23):2700–2709PubMedCrossRef
13.
go back to reference Gruber HE, Gordon B, Williams C et al (2007) Vertebral endplate and disc changes in the aging sand rat lumbar spine: cross-sectional analyses of a large male and female population. Spine 32(23):2529–2536PubMedCrossRef Gruber HE, Gordon B, Williams C et al (2007) Vertebral endplate and disc changes in the aging sand rat lumbar spine: cross-sectional analyses of a large male and female population. Spine 32(23):2529–2536PubMedCrossRef
14.
go back to reference Roberts S, Menage J, Urban JPG (1989) Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine 14:166–174PubMedCrossRef Roberts S, Menage J, Urban JPG (1989) Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine 14:166–174PubMedCrossRef
15.
go back to reference Setton LA, Zhu W, Weidenbaum M et al (1993) Compressive properties of the cartilaginous end-plate of the baboon lumbar spine. J Orthop Res 11:228–239PubMedCrossRef Setton LA, Zhu W, Weidenbaum M et al (1993) Compressive properties of the cartilaginous end-plate of the baboon lumbar spine. J Orthop Res 11:228–239PubMedCrossRef
16.
go back to reference Bernick S, Cailliet R (1982) Vertebral end-plate changes with aging of human vertebrae. Spine 7(2):97–102PubMedCrossRef Bernick S, Cailliet R (1982) Vertebral end-plate changes with aging of human vertebrae. Spine 7(2):97–102PubMedCrossRef
17.
go back to reference Roberts S, Menage J, Eisenstein SM (1993) The cartilage end-plate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res 11:747–757PubMedCrossRef Roberts S, Menage J, Eisenstein SM (1993) The cartilage end-plate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res 11:747–757PubMedCrossRef
18.
go back to reference Gruber HE, Ashraf N, Kilburn J, Williams C, Norton HJ, Gordon BE, Hanley EJ (2005) Vertebral endplate architecture and vascularization: application of micro-computerized tomography, a vascular tracer, and immunocytochemistry in analyses of disc degeneration in the aging sand rat. Spine 30(23):2593–2600PubMedCrossRef Gruber HE, Ashraf N, Kilburn J, Williams C, Norton HJ, Gordon BE, Hanley EJ (2005) Vertebral endplate architecture and vascularization: application of micro-computerized tomography, a vascular tracer, and immunocytochemistry in analyses of disc degeneration in the aging sand rat. Spine 30(23):2593–2600PubMedCrossRef
19.
go back to reference Wang Y, Videman T, Battie MC (2012) ISSLS prize winner: lumbar vertebral endplate lesions: associations with disc degeneration and back pain history. Spine 37(17):1490–1496PubMedCrossRef Wang Y, Videman T, Battie MC (2012) ISSLS prize winner: lumbar vertebral endplate lesions: associations with disc degeneration and back pain history. Spine 37(17):1490–1496PubMedCrossRef
20.
go back to reference Buser Z, Kuelling F, Liu J et al (2011) Biological and biomechanical effects of fibrin injection into porcine intervertebral discs. Spine (Phila Pa 1976) 36:E1201–E1209CrossRef Buser Z, Kuelling F, Liu J et al (2011) Biological and biomechanical effects of fibrin injection into porcine intervertebral discs. Spine (Phila Pa 1976) 36:E1201–E1209CrossRef
21.
go back to reference Melrose J, Shu C, Young C et al (2012) Mechanical destabilisation induced by controlled annular incision of the intervertebral disc dysregulates metalloproteinase expression and induces disc degeneration. Spine (Phila Pa 1976) 37(1):18–25CrossRef Melrose J, Shu C, Young C et al (2012) Mechanical destabilisation induced by controlled annular incision of the intervertebral disc dysregulates metalloproteinase expression and induces disc degeneration. Spine (Phila Pa 1976) 37(1):18–25CrossRef
22.
go back to reference Liang QQ, Cui XJ, Xi ZJ, Bian Q, Hou W, Zhao YJ, Shi Q, Wang YJ (2011) Prolonged upright posture induces degenerative changes in intervertebral discs of rat cervical spine. Spine (Phila Pa 1976) 36:E14–E19CrossRef Liang QQ, Cui XJ, Xi ZJ, Bian Q, Hou W, Zhao YJ, Shi Q, Wang YJ (2011) Prolonged upright posture induces degenerative changes in intervertebral discs of rat cervical spine. Spine (Phila Pa 1976) 36:E14–E19CrossRef
23.
go back to reference Wang YJ, Shi Q, Lu WW et al (2006) Cervical intervertebral disc degeneration induced by unbalanced dynamic and static forces: a novel in vivo rat model. Spine 31(14):1532–1538PubMedCrossRef Wang YJ, Shi Q, Lu WW et al (2006) Cervical intervertebral disc degeneration induced by unbalanced dynamic and static forces: a novel in vivo rat model. Spine 31(14):1532–1538PubMedCrossRef
24.
go back to reference Laing AC, Cox R, Tetzlaff W et al (2011) Effects of advanced age on the morphometry and degenerative state of the cervical spine in a rat model. Anat Rec 294:1326–1336CrossRef Laing AC, Cox R, Tetzlaff W et al (2011) Effects of advanced age on the morphometry and degenerative state of the cervical spine in a rat model. Anat Rec 294:1326–1336CrossRef
25.
go back to reference Han B, Zhu K, Li FC et al (2008) A simple disc degeneration model induced by percutaneous needle puncture in the rat tail. Spine 33(18):1925–1934PubMedCrossRef Han B, Zhu K, Li FC et al (2008) A simple disc degeneration model induced by percutaneous needle puncture in the rat tail. Spine 33(18):1925–1934PubMedCrossRef
26.
go back to reference Moore RJ, Vernon-Roberts B, Fraser RD et al (1996) The origin and fate of herniated lumbar intervertebral disc tissue. Spine 21(18):2149–2155PubMedCrossRef Moore RJ, Vernon-Roberts B, Fraser RD et al (1996) The origin and fate of herniated lumbar intervertebral disc tissue. Spine 21(18):2149–2155PubMedCrossRef
27.
go back to reference Schmid G, Witteler A, Willburger R et al (2004) Lumbar disk herniation: correlation of histologic findings with marrow signal intensity changes in vertebral endplates at MR imaging. Radiology 231(2):352–358PubMedCrossRef Schmid G, Witteler A, Willburger R et al (2004) Lumbar disk herniation: correlation of histologic findings with marrow signal intensity changes in vertebral endplates at MR imaging. Radiology 231(2):352–358PubMedCrossRef
28.
go back to reference Willburger RE, Ehiosun UK, Kuhnen C et al (2004) Clinical symptoms in lumbar disc herniations and their correlation to the histological composition of the extruded disc material. Spine 29(15):1655–1661PubMedCrossRef Willburger RE, Ehiosun UK, Kuhnen C et al (2004) Clinical symptoms in lumbar disc herniations and their correlation to the histological composition of the extruded disc material. Spine 29(15):1655–1661PubMedCrossRef
29.
go back to reference Rajasekaran S, Bajaj N, Tubaki V et al (2013) The anatomy of failure in lumbar disc herniation: an in vivo, multimodal, prospective study of 181 subjects. Spine 38(17):1491–1500PubMedCrossRef Rajasekaran S, Bajaj N, Tubaki V et al (2013) The anatomy of failure in lumbar disc herniation: an in vivo, multimodal, prospective study of 181 subjects. Spine 38(17):1491–1500PubMedCrossRef
30.
go back to reference Stokes IA, Iatridis JC (2004) Mechanical conditions that accelerate intervertebral disc degeneration: overload versus immobilization. Spine 29(23):2724–2732PubMedCrossRef Stokes IA, Iatridis JC (2004) Mechanical conditions that accelerate intervertebral disc degeneration: overload versus immobilization. Spine 29(23):2724–2732PubMedCrossRef
31.
go back to reference Laffosse JM, Accadbled F, Molinier F et al (2010) Correlations between effective permeability and marrow contact channels surface of vertebral endplates. J Orthop Res 28(9):1229–1234PubMedCrossRef Laffosse JM, Accadbled F, Molinier F et al (2010) Correlations between effective permeability and marrow contact channels surface of vertebral endplates. J Orthop Res 28(9):1229–1234PubMedCrossRef
32.
go back to reference Bian Q, Liang QQ, Wan C, Hou W et al (2011) Prolonged upright posture induces calcified hypertrophy in the cartilage end plate in rat lumbar spine. Spine 36(24):2011–2020PubMedCrossRef Bian Q, Liang QQ, Wan C, Hou W et al (2011) Prolonged upright posture induces calcified hypertrophy in the cartilage end plate in rat lumbar spine. Spine 36(24):2011–2020PubMedCrossRef
33.
go back to reference Chen B, Fellenberg J, Wang H et al (2005) Occurrence and regional distribution of apoptosis in scoliotic discs. Spine 30(5):519–524PubMedCrossRef Chen B, Fellenberg J, Wang H et al (2005) Occurrence and regional distribution of apoptosis in scoliotic discs. Spine 30(5):519–524PubMedCrossRef
34.
go back to reference Ariga K, Miyamoto S, Nakase T et al (2001) The relationship between apoptosis of endplate chondrocytes and aging and degeneration of the intervertebral disc. Spine 26(22):2414–2420PubMedCrossRef Ariga K, Miyamoto S, Nakase T et al (2001) The relationship between apoptosis of endplate chondrocytes and aging and degeneration of the intervertebral disc. Spine 26(22):2414–2420PubMedCrossRef
35.
go back to reference Ding Y, Jiang J, Zhou J et al (2013) Effects of imbalance of dynamic and static forces on the disc degeneration of cervical spine at different levels in rats: a micro-CT morphology and histology study. Chin J Spine Spinal Cord 7:638–643 Ding Y, Jiang J, Zhou J et al (2013) Effects of imbalance of dynamic and static forces on the disc degeneration of cervical spine at different levels in rats: a micro-CT morphology and histology study. Chin J Spine Spinal Cord 7:638–643
Metadata
Title
The effects of osteoporosis and disc degeneration on vertebral cartilage endplate lesions in rats
Authors
Yin Ding
Jie Jiang
Jian Zhou
Xiuhua Wu
Zhiping Huang
Jianting Chen
Qingan Zhu
Publication date
01-09-2014
Publisher
Springer Berlin Heidelberg
Published in
European Spine Journal / Issue 9/2014
Print ISSN: 0940-6719
Electronic ISSN: 1432-0932
DOI
https://doi.org/10.1007/s00586-014-3324-9

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