Exploring the Effects of Hypermineralisation in Bone Tissue by Using an Extreme Biological Example

Zioupos, Peter; Currey, John D.; Casinos, Adriá

doi:10.3109/03008200009005292

Cited by 70 publications

(55 citation statements)

References 27 publications

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“…Relative proportions were determined by percentage wet mass. Comparative data were obtained from previous publications (Currey, 2002;Macesic and Summers, 2012;Porter et al, 2006;Toppe et al, 2007;Zioupos et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish

Cohen

Dean

Shipov

et al. 2012

Journal of Experimental Biology

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SUMMARYThe histological diversity of the skeletal tissues of fishes is impressive compared with that of other vertebrate groups, yet our understanding of the functional consequences of this diversity is limited. In particular, although it has been known since the mid1800s that a large number of fish species possess acellular bones, the mechanical advantages and consequences of this structural characteristic -and therefore the nature of the evolution of this feature -remain unclear. Although several studies have examined the material properties of fish bone, these have used a variety of techniques and there have been no direct contrasts of acellular and cellular bone. We report on a comparison of the structural and mechanical properties of the ribs and opercula between two freshwater fish -the common carp Cyprinus carpio (a fish with cellular bone) and the tilapia Oreochromis aureus (a fish with acellular bone). We used light microscopy to show that the bones in both fish species exhibit poor blood supply and possess discrete tissue zones, with visible layering suggesting differences in the underlying collagen architecture. We performed identical micromechanical testing protocols on samples of the two bone types to determine the mechanical properties of the bone material of opercula and ribs. Our data support the consensus of literature values, indicating that Youngʼs moduli of cellular and acellular bones are in the same range, and lower than Youngʼs moduli of the bones of mammals and birds. Despite these similarities in mechanical properties between the bone tissues of the fish species tested here, cellular bone had significantly lower mineral content than acellular bone; furthermore, the percentage ash content and bone mineral density values (derived from micro-CT scans) show that the bone of these fishes is less mineralized than amniote bone. Although we cannot generalize from our data to the numerous remaining teleost species, the results presented here suggest that while cellular and acellular fish bone may perform similarly from a mechanical standpoint, there are previously unappreciated differences in the structure and composition of these bone types.

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Section: Discussionmentioning

confidence: 99%

Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish

Cohen

Dean

Shipov

et al. 2012

Journal of Experimental Biology

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“…7(b) hint that the compositional adaptation of bone material within a long bone fits the same paradigm as that of specialized functionally adapted bones from different creatures (i.e., bulla, antler, etc.). 1,2,7 If the composition of bone is an independent design parameter of bone matrix, then understanding how regions of bone (that are only separated by a few millimeters) can have such large variations in composition will be of interest. The cues (be they genetic or local) for osteoblast matrix synthesis may present novel therapeutic targets for controlling bone composition and, thus, bone's material properties.…”

Section: Limitations and Future Directionsmentioning

confidence: 99%

“…For example, a variety of human, bovine, leopard, brown bear, roe deer, king penguin, polar bear, and wallaby limb bones have the Young's modulus in the range of 16.7 to 22.9 GPa. 1,[4][5][6][7] Other studies, however, have shown that even within a single bone, the mechanical properties of the cortical bone material can have measurable site-specific variations and that these differences can be dependent upon anatomical position. Mechanical and ultrasonic studies of elastic moduli and fracture stresses have been reported for many bone samples, including human, canine, and bovine femora, equine metacarpal bones, and bovine tibiae.…”

Section: Introductionmentioning

confidence: 99%

Functional adaptation of long bone extremities involves the localized “tuning” of the cortical bone composition; evidence from Raman spectroscopy

et al. 2014

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Abstract. In long bones, the functional adaptation of shape and structure occurs along the whole length of the organ. This study explores the hypothesis that adaptation of bone composition is also site-specific and that the mineral-to-collagen ratio of bone (and, thus, its mechanical properties) varies along the organ's length. Raman spectroscopy was used to map the chemical composition of long bones along their entire length in fine spatial resolution (1 mm), and then biochemical analysis was used to measure the mineral, collagen, water, and sulfated glycosaminoglycan content where site-specific differences were seen. The results show that the mineral-to-collagen ratio of the bone material in human tibiae varies by <5% along the mid-shaft but decreases by >10% toward the flared extremities of the bone. Comparisons with long bones from other large animals (horses, sheep, and deer) gave similar results with bone material composition changing across tens of centimeters. The composition of the bone apatite also varied with the phosphate-to-carbonate ratio decreasing toward the ends of the tibia. The data highlight the complexity of adaptive changes and raise interesting questions about the biochemical control mechanisms involved. In addition to their biological interest, the data provide timely information to researchers developing Raman spectroscopy as a noninvasive tool for measuring bone composition in vivo (particularly with regard to sampling and measurement protocol).

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“…Its extremely high density and mineral content explain why it is the mechanical properties of the hypermineralized rostrum that have been most studied. It was reported that the rostrum of M. densirostris has a Vickers hardness of ~223, Young's modulus up to 46.9 GPa, and bending strength up to 59.0 MPa in the longitudinal direction, which makes it the stiffest and hardest of all bones [17,18]. Several potential functions, e.g., to aid in echolocation, combat, and deep diving, have been discussed in previous literature [19][20][21][22][23].…”

Section: Introductionmentioning

confidence: 99%

Hypermineralized whale rostrum as the exemplar for bone mineral

Li¹,

Pasteris²,

Novack³

2013

Connect Tissue Res

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Although bone is a nanocomposite of mineral and collagen, mineral has been the more elusive component to study. A standard for bone mineral clearly is needed. We hypothesized that the most natural, least-processed bone mineral could be retrieved from the most highly mineralized bone. We therefore studied the rostrum of the toothed whale Mesoplodon densirostris, which has the densest recognized bone. Essential to establishment of a standard for bone mineral is documentation that the proposed tissue is bone-like in all properties except for its remarkably high concentration of mineral. Transmitted-light microscopy of unstained sections of rostral material shows normal bone morphology in osteon geometry, lacunae concentration, and vasculature development. Stained sections reveal extremely low density of thin collagen fibers throughout most of the bone, but enrichment in and thicker collagen fibers around vascular holes and in a minority of osteons. FE-SEM shows the rostrum to consist mostly of dense mineral prisms. Most rostral areas have the same chemical-structural features, Raman spectroscopically dominated by strong bands at ~962 cm −1 and weak bands at ~2940 cm −1 . Spectral features indicate that the rostrum is composed mainly of the calcium phosphate mineral apatite and has only about 4 wt.% organic content. The degree of carbonate substitution (~8.5 wt.% carbonate) in the apatite is in the upper range found in most types of bone. We conclude that, despite its enamel-like extraordinarily high degree of mineralization, the rostrum is in all other features bone-like. Its mineral component is the long-sought uncontaminated, unaltered exemplar of bone mineral.

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Exploring the Effects of Hypermineralisation in Bone Tissue by Using an Extreme Biological Example

Cited by 70 publications

References 27 publications

Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish

Comparison of structural, architectural and mechanical aspects of cellular and acellular bone in two teleost fish

Functional adaptation of long bone extremities involves the localized “tuning” of the cortical bone composition; evidence from Raman spectroscopy

Hypermineralized whale rostrum as the exemplar for bone mineral

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