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

Tyler W. Herod; Samuel P. Veres

doi:10.1007/s00586-019-06223-7

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

Tyler W. Herod, Samuel P. Veres

Medicine

Medicine

Research output: Contribution to journal › Article › peer-review

2 Citations (Scopus)

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.[Figure not available: see fulltext.]

Original language	English
Pages (from-to)	670-685
Number of pages	16
Journal	European Spine Journal
Volume	29
Issue number	4
DOIs	https://doi.org/10.1007/s00586-019-06223-7
Publication status	Published - Apr 1 2020

Bibliographical note

Funding Information:
This work was supported by a grant to SPV from the Nova Scotia Health Research Foundation. TWH acknowledges stipend funding support from the Natural Sciences and Engineering Research Council of Canada (NSERC). We acknowledge the support of the Canada Foundation for Innovation, the Atlantic Innovation Fund, and other partners which fund the Facilities for Materials Characterization, managed by the Clean Technologies Research Institute, Dalhousie University.

Funding Information:
This work was supported by a grant to SPV from the Nova Scotia Health Research Foundation. TWH acknowledges stipend funding support from the Natural Sciences and Engineering Research Council of Canada (NSERC). We acknowledge the support of the Canada Foundation for Innovation, the Atlantic Innovation Fund, and other partners which fund the Facilities for Materials Characterization, managed by the Clean Technologies Research Institute, Dalhousie University.

Publisher Copyright:
© 2019, Springer-Verlag GmbH Germany, part of Springer Nature.

ASJC Scopus Subject Areas

Surgery
Orthopedics and Sports Medicine

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

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10.1007/s00586-019-06223-7

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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. / Herod, Tyler W.; Veres, Samuel P.
In: European Spine Journal, Vol. 29, No. 4, 01.04.2020, p. 670-685.

Research output: Contribution to journal › Article › peer-review

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title = "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",

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{\textquoteright} 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.[Figure not available: see fulltext.]",

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note = "Funding Information: This work was supported by a grant to SPV from the Nova Scotia Health Research Foundation. TWH acknowledges stipend funding support from the Natural Sciences and Engineering Research Council of Canada (NSERC). We acknowledge the support of the Canada Foundation for Innovation, the Atlantic Innovation Fund, and other partners which fund the Facilities for Materials Characterization, managed by the Clean Technologies Research Institute, Dalhousie University. Funding Information: This work was supported by a grant to SPV from the Nova Scotia Health Research Foundation. TWH acknowledges stipend funding support from the Natural Sciences and Engineering Research Council of Canada (NSERC). We acknowledge the support of the Canada Foundation for Innovation, the Atlantic Innovation Fund, and other partners which fund the Facilities for Materials Characterization, managed by the Clean Technologies Research Institute, Dalhousie University. Publisher Copyright: {\textcopyright} 2019, Springer-Verlag GmbH Germany, part of Springer Nature.",

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N1 - Funding Information: This work was supported by a grant to SPV from the Nova Scotia Health Research Foundation. TWH acknowledges stipend funding support from the Natural Sciences and Engineering Research Council of Canada (NSERC). We acknowledge the support of the Canada Foundation for Innovation, the Atlantic Innovation Fund, and other partners which fund the Facilities for Materials Characterization, managed by the Clean Technologies Research Institute, Dalhousie University. Funding Information: This work was supported by a grant to SPV from the Nova Scotia Health Research Foundation. TWH acknowledges stipend funding support from the Natural Sciences and Engineering Research Council of Canada (NSERC). We acknowledge the support of the Canada Foundation for Innovation, the Atlantic Innovation Fund, and other partners which fund the Facilities for Materials Characterization, managed by the Clean Technologies Research Institute, Dalhousie University. Publisher Copyright: © 2019, Springer-Verlag GmbH Germany, part of Springer Nature.

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N2 - 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.[Figure not available: see fulltext.]

AB - 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.[Figure not available: see fulltext.]

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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

Abstract

Bibliographical note

ASJC Scopus Subject Areas

PubMed: MeSH publication types

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