Three-Dimensional Observation of Collagen Framework of Lumbar Intervertebral Discs

Inoue, Hajime; Takeda, Tetsuaki

doi:10.3109/17453677508989283

Cited by 98 publications

(44 citation statements)

References 9 publications

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“…Chemical fixation in this extended state followed by decalcification then enabled us to show microscopically and ultrastructurally the existence of discrete nodal insertions into the cartilaginous endplate and confirmed the existence of actual structural integration between the nucleus and endplate. These findings contrast with the more widely held view that the inner nucleus is a largely unstructured gelatinous substance which possesses little or no structural cohesion with its surroundings [3][4][5].…”

Section: Introductioncontrasting

confidence: 90%

Influence of maturity on nucleus–endplate integration in the ovine lumbar spine

2014

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Purpose Recent investigations using an ovine spine model have established that the disc nucleus contains a highly convoluted fibre network with endplate-to-endplate connectivity, this connectivity being achieved via distinctive nodal attachment points. The purpose of this study was to investigate how this nodal anchoring system might be influenced by maturation. Methods Lumbar motion segments were dissected from newborn, 3, 12 months and fully mature ovine animals, subjected to a novel annular ring-severing procedure to remove the strain-limiting influence of the annulus, then either mechanically tested to destruction or examined microstructurally and ultrastructurally. The morphology of the nodes and their linear density within the relatively thin section planes were analysed to provide a basis for comparison between the four age groups. Results Mechanical testing following ring severing revealed that the remaining nuclear material in all samples, irrespective of maturity, had the ability to transmit a substantial load from endplate to endplate. Imaging of the ring-severed samples from all age groups in their stretched, but unruptured state revealed the presence of axially aligned fibrosity in the nucleus region consistent with endplate-to-endplate connectivity. Endplate insertion nodes were observed in all age groups. Ultrastructural examination revealed that the fibrillar architecture of these nodes in the newborn discs was similar to that observed in the nodes of mature discs. However, there was a rapid increase in their linear density between birth and 3 months, after which this remained constant. Conclusions The nodal attachment points identified previously in mature ovine discs are also present in newborn, and 3-and 12-month-old animals with an initial rapid increase in their linear density between birth and 3 months, after which it remained constant. The size and morphology of the attachment points were similar for all ages. Our study suggests that the increase in nodal density in the ovine disc endplate is part of an adaptive response to the loading environment that the disc is exposed to from birth to maturity.

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Section: Introductioncontrasting

confidence: 90%

Influence of maturity on nucleus–endplate integration in the ovine lumbar spine

2014

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“…The organisation of collagen in the annulus fi brosus of the mature IVD is well documented (Inoue and Takeda, 1975;Hashizume, 1980;Inoue, 1981;Hickey and Hukins, 1980;Hukins and Meakin, 2000). To our knowledge this is the fi rst study that has examined, at both light and electron microscopic levels, (i) how the organisation of collagen within the distinct discal tissues becomes established during foetal development, and (ii) the roles that class I and II SLRPs may play in this process.…”

Section: Discussionmentioning

confidence: 99%

“…It consists of a nested series of circumferential coaxial lamellae that enclose the nucleus pulposus of the disc laterally, whilst uniting adjacent vertebral bodies via their endplates rostro-caudally (Peacock 1951a,b;Walmsley, 1953;Inoue and Takeda, 1975;Hashizume, 1980;Inoue, 1981). The lamellae are composed largely of collagen fi bre bundles, with type I collagen predominating in the outermost annulus and type II collagen making up most of the inner annular lamellae (Eyre and Muir, 1977).…”

Section: Introductionmentioning

confidence: 99%

Collagen fibrillogenesis in the development of the annulus fibrosus of the intervertebral disc

Hayes

Isaacs²,

Hughes³

et al. 2011

eCM

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The annulus fi brosus of the intervertebral disc is a complex, radial-ply connective tissue consisting of concentric lamellae of oriented collagen. Whilst much is known of the structure of the mature annulus, less is known of how its complex collagenous architecture becomes established; an understanding of which could inform future repair/ regenerative strategies. Here, using a rat disc developmental series, we describe events in the establishment of the collagenous framework of the annulus at light and electron microscopic levels and examine the involvement of class I and II small leucine rich proteoglycans (SLRPs) in the matrix assembly process. We show that a period of sustained, ordered matrix deposition follows the initial cellular differentiation/orientation phase within the foetal disc. Fibrillar matrix is deposited from recesses within the plasma membrane into compartments of interstitial space within the outer annulus -the orientation of the secreted collagen refl ecting the initial cellular orientation of the laminae. Medially, we demonstrate the development of a reinforcing 'cage' of collagen fi bre bundles around the foetal nucleus pulpous. This derives from the fusion of collagen bundles between presumptive end-plate and inner annulus. By birth, the distinct collagenous architectures are established and the disc undergoes considerable enlargement to maturity. We show that fi bromodulin plays a prominent role in foetal development of the annulus and its attachment to vertebral bodies. With the exception of keratocan, the other SLRPs appear associated more with cartilage development within the vertebral column, but all become more prominent within the disc during its growth and differentiation.

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“…Other studies utilize X-ray diffraction (Hickey and Hukins 1980), whereby this method provides only little or no spatial information. Inoue (1981) and Inoue and Takeda (1975) have used scanning electron microscopy to examine the structure of the anulus fibrosus. These works are concerned with descriptions of the morphology of observed collagen fibrils rather than with a quantitative investigation of lamellar fiber angles.…”

Section: Introductionmentioning

confidence: 99%

Single lamellar mechanics of the human lumbar anulus fibrosus

Holzapfel

Schulze-Bauer

Feigl

et al. 2004

Biomech Model Mechanobiol

391

285

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The mechanical behavior of the entire anulus fibrosus is determined essentially by the tensile properties of its lamellae, their fiber orientations, and the regional variation of these quantities. Corresponding data are rare in the literature. The paper deals with an in vitro study of single lamellar anulus lamellae and aims to determine (i) their tensile response and regional variation, and (ii) the orientation of lamellar collagen fibers and their regional variation. Fresh human body-disc-body units (L1-L2, n=11) from cadavers were cut midsagittally producing two hemidisc units. One hemidisc was used for the preparation of single lamellar anulus specimens for tensile testing, while the other one was used for the investigation of the lamellar fiber orientation. Single lamellar anulus specimens with adjacent bone fragments were isolated from four anatomical regions: superficial and deep lamellae (3.9+/-0.21 mm, mean +/- SD, apart from the outer boundary surface of the anulus fibrosus) at ventro-lateral and dorsal positions. The specimens underwent cyclic uniaxial tensile tests at three different strain rates in 0.15 mol/l NaCl solution at 37 degrees C, whereby the lamellar fiber direction was aligned with the load axis. For the characterization of the tensile behavior three moduli were calculated: E(low) (0-0.1 MPa), E(medium) (0.1-0.5 MPa) and E(high) (0.5-1 MPa). Additionally, specimens were tested with the load axis transverse to the fiber direction. From the second hemidisc fiber angles with respect to the horizontal plane were determined photogrammetrically from images taken at six circumferential positions from ventral to dorsal and at three depth levels. Tensile moduli along the fiber direction were in the range of 28-78 MPa (regional mean values). Superficial lamellae have larger E(medium) (p=0.017) and E(high) (p=0.012) than internal lamellae, and the mean value of superficial lamellae is about three times higher than that of deep lamellae. Tensile moduli of ventro-lateral lamellae do not differ significantly from the tensile moduli of dorsal lamellae, and E(low) is generally indifferent with respect to the anatomical region. Tensile moduli transverse to the fiber direction were about two orders of magnitude smaller (0.22+/-0.2 MPa, mean +/- SD, n=5). Tensile properties are not correlated significantly with donor age. Only small viscoelastic effects were observed. The regional variation of lamellar fiber angle phi is described appropriately by a regression line |phi|=23.2 + 0.130 x alpha (r(2)=0.55, p<0.001), where alpha is the polar angle associated with the circumferential position. The single anulus lamella may be seen as the elementary structural unit of the anulus fibrosus, and exhibits marked anisotropy and distinct regional variation of tensile properties and fiber angles. These features must be considered for appropriate physical and numerical modeling of the anulus fibrosus.

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Three-Dimensional Observation of Collagen Framework of Lumbar Intervertebral Discs

Cited by 98 publications

References 9 publications

Influence of maturity on nucleus–endplate integration in the ovine lumbar spine

Influence of maturity on nucleus–endplate integration in the ovine lumbar spine

Collagen fibrillogenesis in the development of the annulus fibrosus of the intervertebral disc

Single lamellar mechanics of the human lumbar anulus fibrosus

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