Skip to main content
Erschienen in: European Spine Journal 4/2020

25.11.2019 | Original Article

ISSLS PRIZE IN BASIC SCIENCE 2020: Beyond microstructure—circumferential specialization within the lumbar intervertebral disc annulus extends to collagen nanostructure, with counterintuitive relationships to macroscale material properties

Erschienen in: European Spine Journal | Ausgabe 4/2020

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To determine whether the annulus of lumbar intervertebral discs contains circumferential specialization in collagen nanostructure and assess whether this coincides with functional differences in macroscale material properties.

Methods

Anterior and posterior disc wall samples were prepared from 38 mature ovine lumbar segments. Regional differences in molecular thermal stability and intermolecular network integrity of the annulus’ tension-bearing collagen fibres were examined with hydrothermal isometric tension (HIT) analysis, with and without preceding NaBH4 treatment to stabilize labile crosslinks. Energetics of collagen denaturation were studied by differential scanning calorimetry (DSC). Tensile mechanics of annular lamellae were studied using oblique sagittal bone-disc-bone samples loaded to rupture. Annular failure characteristics of the ruptured test segments were compared via microscopy of serial sections.

Results

HIT showed that tension-bearing collagen fibres of the posterior annulus were composed of collagen molecules with significantly greater thermal stability and intermolecular network integrity than those of the anterior annulus. NaBH4 treatment confirmed that labile intermolecular crosslinks did not significantly contribute to network integrity in either region. Regional differences seen in DSC were smaller than those observed in HIT, indicating structural similarities in annular collagen outside of the main fibre bundles. Mechanical testing showed that the posterior annulus was significantly weaker than the anterior annulus. For both regions, ultimate tensile strengths of annular fibres were significantly greater than those previously reported. Ruptures in both regions were predominantly due to annular failure.

Conclusion

Specializations in collagen nanostructure exist between different circumferential regions of the annulus and coincide with significant differences in material properties.

Graphic abstract

These slides can be retrieved under Electronic Supplementary Material.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
6.
Zurück zum Zitat Tsuji H, Hirano N, Ohshima H et al (1993) Structural variation of the anterior and posterior anulus fibrosus in the development of human lumbar intervertebral disc. A risk factor for intervertebral disc rupture. Spine 18:204–210CrossRef Tsuji H, Hirano N, Ohshima H et al (1993) Structural variation of the anterior and posterior anulus fibrosus in the development of human lumbar intervertebral disc. A risk factor for intervertebral disc rupture. Spine 18:204–210CrossRef
9.
Zurück zum Zitat Moore RJ, Vernon-Roberts B, Fraser RD et al (1996) The origin and fate of herniated lumbar intervertebral disc tissue. Spine 21:2149–2155CrossRef Moore RJ, Vernon-Roberts B, Fraser RD et al (1996) The origin and fate of herniated lumbar intervertebral disc tissue. Spine 21:2149–2155CrossRef
10.
Zurück zum Zitat Osti OL, Vernon-Roberts B, Moore R, Fraser RD (1992) Annular tears and disc degeneration in the lumbar spine. A post-mortem study of 135 discs. J Bone Joint Surg Br 74:678–682CrossRef Osti OL, Vernon-Roberts B, Moore R, Fraser RD (1992) Annular tears and disc degeneration in the lumbar spine. A post-mortem study of 135 discs. J Bone Joint Surg Br 74:678–682CrossRef
19.
Zurück zum Zitat Reid JE, Meakin JR, Robins SP et al (2002) Sheep lumbar intervertebral discs as models for human discs. Clin Biomech (Bristol Avon) 17:312–314CrossRef Reid JE, Meakin JR, Robins SP et al (2002) Sheep lumbar intervertebral discs as models for human discs. Clin Biomech (Bristol Avon) 17:312–314CrossRef
20.
Zurück zum Zitat Lee JM, Pereira CA, Abdulla D et al (1995) A multi-sample denaturation temperature tester for collagenous biomaterials. Med Eng Phys 17:115–121CrossRef Lee JM, Pereira CA, Abdulla D et al (1995) A multi-sample denaturation temperature tester for collagenous biomaterials. Med Eng Phys 17:115–121CrossRef
21.
Zurück zum Zitat Wells SM, Adamson SL, Langille BL, Lee JM (1998) Thermomechanical analysis of collagen crosslinking in the developing ovine thoracic aorta. Biorheology 35:399–414CrossRef Wells SM, Adamson SL, Langille BL, Lee JM (1998) Thermomechanical analysis of collagen crosslinking in the developing ovine thoracic aorta. Biorheology 35:399–414CrossRef
22.
Zurück zum Zitat Weiderhorn NM, Reardon GV (1952) Studies concerned with the structure of collagen. II. Stress-strain behavior of thermally contracted collagen. J Polym Sci 9:315–325CrossRef Weiderhorn NM, Reardon GV (1952) Studies concerned with the structure of collagen. II. Stress-strain behavior of thermally contracted collagen. J Polym Sci 9:315–325CrossRef
24.
Zurück zum Zitat Le Lous M, Cohen-Solal L, Allain JC et al (1985) Age related evolution of stable collagen reticulation in human skin. Connect Tissue Res 13:145–155CrossRef Le Lous M, Cohen-Solal L, Allain JC et al (1985) Age related evolution of stable collagen reticulation in human skin. Connect Tissue Res 13:145–155CrossRef
25.
Zurück zum Zitat Bailey AJ, Lister D (1968) Thermally labile cross-links in native collagen. Nature 220:280–281CrossRef Bailey AJ, Lister D (1968) Thermally labile cross-links in native collagen. Nature 220:280–281CrossRef
26.
Zurück zum Zitat Avery NC, Bailey AJ (2008) Restraining cross-links responsible for the mechanical properties of collagen fibers: natural and artificial. In: Fratzl P (ed) Collagen structure and mechanics. Springer, Boston, pp 81–110 Avery NC, Bailey AJ (2008) Restraining cross-links responsible for the mechanical properties of collagen fibers: natural and artificial. In: Fratzl P (ed) Collagen structure and mechanics. Springer, Boston, pp 81–110
34.
Zurück zum Zitat Eyre DR, Koob TJ, Van Ness KP (1984) Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. Anal Biochem 137:380–388CrossRef Eyre DR, Koob TJ, Van Ness KP (1984) Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. Anal Biochem 137:380–388CrossRef
35.
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 19:1310–1319CrossRef Skaggs DL, Weidenbaum M, Iatridis JC et al (1994) Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19:1310–1319CrossRef
39.
Zurück zum Zitat Robins SP, Bailey AJ (1973) The chemistry of the collagen cross-links. The characterization of fraction C, a possible artifact produced during the reduction of collagen fibres with borohydride. Biochem J 135:657–665CrossRef Robins SP, Bailey AJ (1973) The chemistry of the collagen cross-links. The characterization of fraction C, a possible artifact produced during the reduction of collagen fibres with borohydride. Biochem J 135:657–665CrossRef
40.
Zurück zum Zitat Bernstein PH, Mechanic GL (1980) A natural histidine-based imminium cross-link in collagen and its location. J Biol Chem 255:10414–10422PubMed Bernstein PH, Mechanic GL (1980) A natural histidine-based imminium cross-link in collagen and its location. J Biol Chem 255:10414–10422PubMed
44.
Zurück zum Zitat Haut RC (1985) The effect of a lathyritic diet on the sensitivity of tendon to strain rate. J Biomech Eng 107:166–174CrossRef Haut RC (1985) The effect of a lathyritic diet on the sensitivity of tendon to strain rate. J Biomech Eng 107:166–174CrossRef
48.
Zurück zum Zitat Le Lous M, Allain JC, Cohen-Solal L, Maroteaux P (1982) The rate of collagen maturation in rat and human skin. Connect Tissue Res 9:253–262CrossRef Le Lous M, Allain JC, Cohen-Solal L, Maroteaux P (1982) The rate of collagen maturation in rat and human skin. Connect Tissue Res 9:253–262CrossRef
49.
Zurück zum Zitat Bailey AJ (1968) Intermediate labile intermolecular crosslinks in collagen fibres. Biochim Biophys Acta 160:447–453CrossRef Bailey AJ (1968) Intermediate labile intermolecular crosslinks in collagen fibres. Biochim Biophys Acta 160:447–453CrossRef
50.
Zurück zum Zitat Torp S, Arridge RGC, Armeniades CD, Baer E (1975) Structure–property relationships in tendon as a function of age. Struct Fibrous Biopolym 26:197–221 Torp S, Arridge RGC, Armeniades CD, Baer E (1975) Structure–property relationships in tendon as a function of age. Struct Fibrous Biopolym 26:197–221
52.
Zurück zum Zitat Ker RF, Alexander R, Bennett MB (1988) Why are mammalian tendons so thick? J Zool 216:309–324CrossRef Ker RF, Alexander R, Bennett MB (1988) Why are mammalian tendons so thick? J Zool 216:309–324CrossRef
56.
Zurück zum Zitat Green TP, Adams MA, Dolan P (1993) Tensile properties of the annulus fibrosus II. Ultimate tensile strength and fatigue life. Eur Spine J 2:209–214CrossRef Green TP, Adams MA, Dolan P (1993) Tensile properties of the annulus fibrosus II. Ultimate tensile strength and fatigue life. Eur Spine J 2:209–214CrossRef
63.
Zurück zum Zitat Ohnmeiss DD, Vanharanta H, Ekholm J (1999) Relation between pain location and disc pathology: a study of pain drawings and CT/discography. Clin J Pain 15:210–217CrossRef Ohnmeiss DD, Vanharanta H, Ekholm J (1999) Relation between pain location and disc pathology: a study of pain drawings and CT/discography. Clin J Pain 15:210–217CrossRef
Metadaten
Titel
ISSLS PRIZE IN BASIC SCIENCE 2020: Beyond microstructure—circumferential specialization within the lumbar intervertebral disc annulus extends to collagen nanostructure, with counterintuitive relationships to macroscale material properties
Publikationsdatum
25.11.2019
Erschienen in
European Spine Journal / Ausgabe 4/2020
Print ISSN: 0940-6719
Elektronische ISSN: 1432-0932
DOI
https://doi.org/10.1007/s00586-019-06223-7

Weitere Artikel der Ausgabe 4/2020

European Spine Journal 4/2020 Zur Ausgabe

Editorial

Editorial

Arthropedia

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

Proximale Humerusfraktur: Auch 100-Jährige operieren?

01.05.2024 DCK 2024 Kongressbericht

Mit dem demographischen Wandel versorgt auch die Chirurgie immer mehr betagte Menschen. Von Entwicklungen wie Fast-Track können auch ältere Menschen profitieren und bei proximaler Humerusfraktur können selbst manche 100-Jährige noch sicher operiert werden.

Sind Frauen die fähigeren Ärzte?

30.04.2024 Gendermedizin Nachrichten

Patienten, die von Ärztinnen behandelt werden, dürfen offenbar auf bessere Therapieergebnisse hoffen als Patienten von Ärzten. Besonders gilt das offenbar für weibliche Kranke, wie eine Studie zeigt.

Notfall-TEP der Hüfte ist auch bei 90-Jährigen machbar

26.04.2024 Hüft-TEP Nachrichten

Ob bei einer Notfalloperation nach Schenkelhalsfraktur eine Hemiarthroplastik oder eine totale Endoprothese (TEP) eingebaut wird, sollte nicht allein vom Alter der Patientinnen und Patienten abhängen. Auch über 90-Jährige können von der TEP profitieren.

Arthroskopie kann Knieprothese nicht hinauszögern

25.04.2024 Gonarthrose Nachrichten

Ein arthroskopischer Eingriff bei Kniearthrose macht im Hinblick darauf, ob und wann ein Gelenkersatz fällig wird, offenbar keinen Unterschied.

Update Orthopädie und Unfallchirurgie

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