Skip to main content
Erschienen in: European Spine Journal 1/2017

10.05.2016 | Original Article

The aging disc: using an ovine model to examine age-related differences in the biomechanical properties of the intralamellar matrix of single lamellae

verfasst von: Danielle M. Stewart, Lauren A. Monaco, Diane E. Gregory

Erschienen in: European Spine Journal | Ausgabe 1/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To determine the effect of age on the biomechanical properties of the intralamellar matrix of single annulus fibrosus (AF) lamellae.

Methods

One intervertebral disc (IVD) was excised from five young (<12 months), five middle-aged (2–4 years) and five older (5–7 years) ovine lumbar spines. From each IVD, a maximum of four single AF lamellae samples were harvested: two from the anterior region and two from the posterior region. Tissues were mounted in a tensile testing apparatus such that tension was applied perpendicular to the orientation of the collagen fibers to isolate the intralamellar matrix. Variables of interest from the stress–strain relationship were: end of toe-region strain and corresponding stress, initial failure stress and strain, and elastic stiffness.

Results

When compared to the middle-aged and old samples, the intralamellar matrix of young AF samples displayed significantly higher stress values at the end of the end of toe-region (p = 0.008) and at initial failure (p = 0.002). Further, the young samples were stiffer than both middle-aged and old samples (p = 0.04).

Conclusions

This study was the first to show that the intralamellar matrix of single AF lamellae is weaker and more compliant in middle-aged and old ovine IVDs compared to young IVDs. These findings are likely a result of the remarkable age-related changes that occur that ultimately weaken the IVD as a whole.
Literatur
1.
Zurück zum Zitat Marchand F, Ahmed AM (1990) Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15:110–402CrossRef Marchand F, Ahmed AM (1990) Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15:110–402CrossRef
2.
Zurück zum Zitat Aguiar DJ, Johnson SL, Oegema TR (1999) Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp Cell Res 246:129–137CrossRefPubMed Aguiar DJ, Johnson SL, Oegema TR (1999) Notochordal cells interact with nucleus pulposus cells: regulation of proteoglycan synthesis. Exp Cell Res 246:129–137CrossRefPubMed
3.
Zurück zum Zitat Gower WE, Pedrini V (1969) Age-related variations in protein polysaccharides from human nucleus and costal cartilage. J Bone Joint Surg 51:1154–1162CrossRefPubMed Gower WE, Pedrini V (1969) Age-related variations in protein polysaccharides from human nucleus and costal cartilage. J Bone Joint Surg 51:1154–1162CrossRefPubMed
4.
Zurück zum Zitat Kandel R, Hamilton D, Séguin C et al (2007) An in vitro tissue model to study the effect of age on nucleus pulposus cells. Eur Spine J 16:2166–2173CrossRefPubMedPubMedCentral Kandel R, Hamilton D, Séguin C et al (2007) An in vitro tissue model to study the effect of age on nucleus pulposus cells. Eur Spine J 16:2166–2173CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Reid JE, Meakin JR, Robins SP et al (2002) Sheep lumbar intervertebral discs as models for human discs. Clin Biomech 17:312–314CrossRef Reid JE, Meakin JR, Robins SP et al (2002) Sheep lumbar intervertebral discs as models for human discs. Clin Biomech 17:312–314CrossRef
6.
Zurück zum Zitat Antoniou J, Steffen T, Nelson F et al (1996) The human lumbar intervertebral disc: evidence for changes in the biosynthesis and denaturation of the extracellular matrix with growth, maturation, ageing and degeneration. J Clin Invest 98:996–1003CrossRefPubMedPubMedCentral Antoniou J, Steffen T, Nelson F et al (1996) The human lumbar intervertebral disc: evidence for changes in the biosynthesis and denaturation of the extracellular matrix with growth, maturation, ageing and degeneration. J Clin Invest 98:996–1003CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Adams MA, Nally D, Dolan P (1996) ‘Stress’ distributions inside intervertebral discs the effects of age and degeneration. J Bone Joint Surg 78:965–972CrossRef Adams MA, Nally D, Dolan P (1996) ‘Stress’ distributions inside intervertebral discs the effects of age and degeneration. J Bone Joint Surg 78:965–972CrossRef
8.
Zurück zum Zitat Roughley PJ (2004) Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine 29:2691–2699CrossRefPubMed Roughley PJ (2004) Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine 29:2691–2699CrossRefPubMed
9.
Zurück zum Zitat Zhao C-Q, Wang L-M, Jiang L-S, Dai L-Y (2007) The cell biology of intervertebral disc aging and degeneration. Ageing Res Rev 6:247–261CrossRefPubMed Zhao C-Q, Wang L-M, Jiang L-S, Dai L-Y (2007) The cell biology of intervertebral disc aging and degeneration. Ageing Res Rev 6:247–261CrossRefPubMed
10.
Zurück zum Zitat Holzapfel G, Schulze-Bauer CJ, Feigl G et al (2005) Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech Model Mechanobiol 3:125–140CrossRefPubMed Holzapfel G, Schulze-Bauer CJ, Feigl G et al (2005) Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech Model Mechanobiol 3:125–140CrossRefPubMed
11.
Zurück zum Zitat Skaggs DL, Weidenbaum M, Iatridis JC et al (1994) Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19:1310–1319CrossRefPubMed Skaggs DL, Weidenbaum M, Iatridis JC et al (1994) Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19:1310–1319CrossRefPubMed
12.
Zurück zum Zitat Tampier C, Drake JD, Callaghan JP, McGill SM (2007) Progressive disc herniation: an investigation of the mechanism using radiologic, histochemical, and microscopic dissection techniques on a porcine model. Spine 32(25):2869–2874CrossRefPubMed Tampier C, Drake JD, Callaghan JP, McGill SM (2007) Progressive disc herniation: an investigation of the mechanism using radiologic, histochemical, and microscopic dissection techniques on a porcine model. Spine 32(25):2869–2874CrossRefPubMed
13.
Zurück zum Zitat Wilke HJ, Kettler A, Wenger KH et al (1997) Anatomy of the sheep spine and its comparison to the human spine. Anat Rec 247:542–555CrossRefPubMed Wilke HJ, Kettler A, Wenger KH et al (1997) Anatomy of the sheep spine and its comparison to the human spine. Anat Rec 247:542–555CrossRefPubMed
14.
Zurück zum Zitat O’Connell GD, Vresilovic EJ, Elliott DM (2007) Comparison of animals used in disc research to human lumbar disc geometry. Spine 32:328–333CrossRefPubMed O’Connell GD, Vresilovic EJ, Elliott DM (2007) Comparison of animals used in disc research to human lumbar disc geometry. Spine 32:328–333CrossRefPubMed
15.
16.
Zurück zum Zitat Schmidt H, Reitmaier S (2013) Is the ovine intervertebral disc a small human one? A finite element model study. J Mech Behav Biomed Mater 17:229–241CrossRefPubMed Schmidt H, Reitmaier S (2013) Is the ovine intervertebral disc a small human one? A finite element model study. J Mech Behav Biomed Mater 17:229–241CrossRefPubMed
17.
Zurück zum Zitat Reutlinger C, Burki A, Brandejsk V et al (2014) Specimen specific parameter identification of ovine lumbar intervertebral discs: On the influence of fibre matrix and fibre–fibre shear interactions. J Mech Behav Biomed Mater 30:279–289CrossRefPubMed Reutlinger C, Burki A, Brandejsk V et al (2014) Specimen specific parameter identification of ovine lumbar intervertebral discs: On the influence of fibre matrix and fibre–fibre shear interactions. J Mech Behav Biomed Mater 30:279–289CrossRefPubMed
18.
Zurück zum Zitat Karakaşli A, Yıldız DV, Kumtepe E et al (2013) Biomechanical comparison of intact lumbar lamb spine and endoscopic discectomized lamb spine. Eklem Hastalik Cerrahisi 24:33–38CrossRefPubMed Karakaşli A, Yıldız DV, Kumtepe E et al (2013) Biomechanical comparison of intact lumbar lamb spine and endoscopic discectomized lamb spine. Eklem Hastalik Cerrahisi 24:33–38CrossRefPubMed
19.
Zurück zum Zitat Hollingsworth NT, Wagner DR (2012) The stress and strain states of the posterior annulus under flexion. Spine 37:E1134–E1139CrossRefPubMed Hollingsworth NT, Wagner DR (2012) The stress and strain states of the posterior annulus under flexion. Spine 37:E1134–E1139CrossRefPubMed
20.
Zurück zum Zitat Gregory DE, Callaghan JP (2011) Does vibration influence the initiation of intervertebral disc herniation? an example of herniation occurrence using a porcine cervical disc model. Spine 36:E225–E231CrossRefPubMed Gregory DE, Callaghan JP (2011) Does vibration influence the initiation of intervertebral disc herniation? an example of herniation occurrence using a porcine cervical disc model. Spine 36:E225–E231CrossRefPubMed
21.
Zurück zum Zitat Iatridis JC, MaClean JJ, Ryan D (2005) Mechanical damage to the intervertebral disc annulus fibrosus subjected to tensile loading. J Biomech 38:557–565CrossRefPubMed Iatridis JC, MaClean JJ, Ryan D (2005) Mechanical damage to the intervertebral disc annulus fibrosus subjected to tensile loading. J Biomech 38:557–565CrossRefPubMed
22.
Zurück zum Zitat Gunning JL, Callaghan JP, Mcgill SM (2001) Spinal posture and prior loading history modulate compressive strength and type of failure in the spine : a biomechanical study using a porcine cervical spine model. Clin Biomech 16:471–480CrossRef Gunning JL, Callaghan JP, Mcgill SM (2001) Spinal posture and prior loading history modulate compressive strength and type of failure in the spine : a biomechanical study using a porcine cervical spine model. Clin Biomech 16:471–480CrossRef
23.
Zurück zum Zitat Costi JJ, Hearn TC, Fazzalari NL (2002) The effect of hydration on the stiffness of intervertebral discs in an ovine model. Clin Biomech 17:446–455CrossRef Costi JJ, Hearn TC, Fazzalari NL (2002) The effect of hydration on the stiffness of intervertebral discs in an ovine model. Clin Biomech 17:446–455CrossRef
24.
Zurück zum Zitat Ebara S, Iatridis JC, Setton LA et al (1996) Tensile properties of the non-degenerate human lumbar annulus fibrosus. Spine 21:452–461CrossRefPubMed Ebara S, Iatridis JC, Setton LA et al (1996) Tensile properties of the non-degenerate human lumbar annulus fibrosus. Spine 21:452–461CrossRefPubMed
25.
Zurück zum Zitat Pezowicz CA, Robertson PA, Broom ND (2005) Intralamellar relationships within the collagenous architecture of the annulus fibrosus imaged in its fully hydrated state. J Anat 207:299–312CrossRefPubMedPubMedCentral Pezowicz CA, Robertson PA, Broom ND (2005) Intralamellar relationships within the collagenous architecture of the annulus fibrosus imaged in its fully hydrated state. J Anat 207:299–312CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Dolan P, Luo J, Pollintine P et al (2013) Intervertebral disc decompression following endplate damage: implications for disc degeneration depend on spinal level and age. Spine 38:1473–1481CrossRefPubMed Dolan P, Luo J, Pollintine P et al (2013) Intervertebral disc decompression following endplate damage: implications for disc degeneration depend on spinal level and age. Spine 38:1473–1481CrossRefPubMed
27.
Zurück zum Zitat Park C, Kim YJ, Lee CS et al (2005) An in vitro animal study of the biomechanical responses of anulus fibrosus with aging. Spine 30:E259–E265CrossRefPubMed Park C, Kim YJ, Lee CS et al (2005) An in vitro animal study of the biomechanical responses of anulus fibrosus with aging. Spine 30:E259–E265CrossRefPubMed
28.
Zurück zum Zitat Beckstein JC, Sen S, Schaer TP et al (2008) Comparison of animal discs used in disc research to human lumbar disc: axial compression mechanics and glycosaminoglycan content. Spine 33:E166–E173CrossRefPubMed Beckstein JC, Sen S, Schaer TP et al (2008) Comparison of animal discs used in disc research to human lumbar disc: axial compression mechanics and glycosaminoglycan content. Spine 33:E166–E173CrossRefPubMed
29.
Zurück zum Zitat Trout JJ, Buckwaltert JA, Moore KC et al (1982) Ultrastructure of the human intervertebral disc. I. changes in notochordal cells with age. Tissue Cell 14:359–369CrossRefPubMed Trout JJ, Buckwaltert JA, Moore KC et al (1982) Ultrastructure of the human intervertebral disc. I. changes in notochordal cells with age. Tissue Cell 14:359–369CrossRefPubMed
30.
Zurück zum Zitat Pazzaglia UE, Salisbury JR (1989) Development and involution of the notochord in the human spine. J R Soc Med 82:413–415PubMedPubMedCentral Pazzaglia UE, Salisbury JR (1989) Development and involution of the notochord in the human spine. J R Soc Med 82:413–415PubMedPubMedCentral
31.
Zurück zum Zitat Weiler C, Nerlich AG, Schaaf R, Bachmeier BE, Wuertz K, Boos N (2010) Immunohistochemical identification of notochordal markers in cells in the aging human lumbar intervertebral disc. Eur Spine J 19:1761–1770CrossRefPubMedPubMedCentral Weiler C, Nerlich AG, Schaaf R, Bachmeier BE, Wuertz K, Boos N (2010) Immunohistochemical identification of notochordal markers in cells in the aging human lumbar intervertebral disc. Eur Spine J 19:1761–1770CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Sun Z, Wang HQ, Liu ZH, Chang L, Chen YF, Zhang YZ, Zhang WL, Gao Y, Wan ZY, Che L, Liu X, Samartzis D, Luo ZJ (2013) Down-regulated CK8 expression in human intervertebral disc degeneration. Int J Med Sci 10:948–956CrossRefPubMedPubMedCentral Sun Z, Wang HQ, Liu ZH, Chang L, Chen YF, Zhang YZ, Zhang WL, Gao Y, Wan ZY, Che L, Liu X, Samartzis D, Luo ZJ (2013) Down-regulated CK8 expression in human intervertebral disc degeneration. Int J Med Sci 10:948–956CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Melrose J, Smith SM, Appleyard RC, Little CB (2008) Aggrecan, versican and type VI collagen are components of annular translamellar crossbridges in the intervertebral disc. Eur Spine J 17:314–324CrossRefPubMed Melrose J, Smith SM, Appleyard RC, Little CB (2008) Aggrecan, versican and type VI collagen are components of annular translamellar crossbridges in the intervertebral disc. Eur Spine J 17:314–324CrossRefPubMed
34.
Zurück zum Zitat Olczyk K (1994) Age-related changes of elastin content in human intervertebral discs. Folia Histochem Cytobiol 32:41–44PubMed Olczyk K (1994) Age-related changes of elastin content in human intervertebral discs. Folia Histochem Cytobiol 32:41–44PubMed
35.
Zurück zum Zitat Smith LJ, Fazzalari NL (2006) Regional variations in the density and arrangement of elastic fibres in the anulus fibrosus of the human lumbar disc. J Anat 209:359–367CrossRefPubMedPubMedCentral Smith LJ, Fazzalari NL (2006) Regional variations in the density and arrangement of elastic fibres in the anulus fibrosus of the human lumbar disc. J Anat 209:359–367CrossRefPubMedPubMedCentral
36.
Zurück zum Zitat Cloyd JM, Elliott DM (2007) Elastin content correlates with human disc degeneration in the anulus fibrosus and nucleus pulposus. Spine 32:1826–1831CrossRefPubMed Cloyd JM, Elliott DM (2007) Elastin content correlates with human disc degeneration in the anulus fibrosus and nucleus pulposus. Spine 32:1826–1831CrossRefPubMed
37.
Zurück zum Zitat Smith LJ, Fazzalari NL (2009) The elastic fibre network of the human lumbar anulus fibrosus: architecture, mechanical function and potential role in the progression of intervertebral disc degeneration. Euro Spine J 18:439–448CrossRef Smith LJ, Fazzalari NL (2009) The elastic fibre network of the human lumbar anulus fibrosus: architecture, mechanical function and potential role in the progression of intervertebral disc degeneration. Euro Spine J 18:439–448CrossRef
38.
Zurück zum Zitat Aufdermaur M (1974) Spinal injuries in juveniles: necropsy findings in twelve cases. J Bone Surg 56B:513–519 Aufdermaur M (1974) Spinal injuries in juveniles: necropsy findings in twelve cases. J Bone Surg 56B:513–519
39.
Zurück zum Zitat Karlsson L, Lundin O, Ekstrom L et al (1974) Injuries in adolescent spine exposed to compressive loads: an experimental cadaveric study. J Spinal Disord 11:501–507 Karlsson L, Lundin O, Ekstrom L et al (1974) Injuries in adolescent spine exposed to compressive loads: an experimental cadaveric study. J Spinal Disord 11:501–507
40.
Zurück zum Zitat Schollum ML, Robertson P, Broom ND (2007) How age influences unravelling morphology of annular lamellae—a study of interfibre cohesivity in the lumbar disc. J Anat 216:310–319CrossRef Schollum ML, Robertson P, Broom ND (2007) How age influences unravelling morphology of annular lamellae—a study of interfibre cohesivity in the lumbar disc. J Anat 216:310–319CrossRef
41.
Zurück zum Zitat Guerin HAL, Elliott DM (2006) Degeneration affects the fiber reorientation of human annulus fibrosus under tensile load. J Biomech 39:1410–1418CrossRefPubMed Guerin HAL, Elliott DM (2006) Degeneration affects the fiber reorientation of human annulus fibrosus under tensile load. J Biomech 39:1410–1418CrossRefPubMed
Metadaten
Titel
The aging disc: using an ovine model to examine age-related differences in the biomechanical properties of the intralamellar matrix of single lamellae
verfasst von
Danielle M. Stewart
Lauren A. Monaco
Diane E. Gregory
Publikationsdatum
10.05.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
European Spine Journal / Ausgabe 1/2017
Print ISSN: 0940-6719
Elektronische ISSN: 1432-0932
DOI
https://doi.org/10.1007/s00586-016-4603-4

Weitere Artikel der Ausgabe 1/2017

European Spine Journal 1/2017 Zur Ausgabe

Arthropedia

Grundlagenwissen der Arthroskopie und Gelenkchirurgie. Erweitert durch Fallbeispiele, Videos und Abbildungen. 
» Jetzt entdecken

Update Orthopädie und Unfallchirurgie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.