Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing

Schmidt, Felix N.; Delsmann, Maximilian M.; Mletzko, Kathrin; Yorgan, Timur Alexander; Hahn, Michael; Siebert, Ursula; Busse, Björn; Oheim, Ralf; Amling, Michael; Rolvien, Tim

doi:10.1098/rspb.2018.1820

Cited by 17 publications

(21 citation statements)

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“…The most surprising finding from this study was the continued mineralization of the interdigitated bone over time following cementing of the tibia. Hyper‐mineralization of bone is known to occur in auditory ossicles and is accompanied by osteocyte death and low‐bone remodeling . Several proteins have been identified as having roles in controlling local matrix mineralization, and osteocyte death through apoptosis or necrosis could release these proteins locally, contributing transiently to local matrix mineralization.…”

Section: Discussionmentioning

confidence: 99%

“…Hypermineralization of bone is known to occur in auditory JOURNAL OF ORTHOPAEDIC RESEARCH ® OCTOBER 2019 ossicles and is accompanied by osteocyte death and lowbone remodeling. 19,20 Several proteins have been identified as having roles in controlling local matrix mineralization, 21 and osteocyte death through apoptosis or necrosis could release these proteins locally, contributing transiently to local matrix mineralization. The hyper-mineralized interdigitated bone found in the current study exhibited extensive osteocyte death and low bone turnover, suggesting that the mechanism of action may be similar to that documented in auditory ossicles.…”

Section: Discussionmentioning

confidence: 99%

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Early Changes in Cement–Bone Fixation Using a Novel Rat Knee Replacement Model

Mann

Miller

Amendola

et al. 2019

Journal Orthopaedic Research

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Trabecular resorption from interdigitated regions between cement and bone has been found in postmortem‐retrieved knee replacements, but the viability of interdigitated bone, and the mechanism responsible for this bone loss is not known. In this work, a Sprague–Dawley (age 12 weeks) rat knee replacement model with an interdigitated cement–bone interface was developed. Morphological and cellular changes in the interdigitated region of the knee replacement over time (0, 2, 6, or 12 weeks) were determined for ovariectomy (OVX) and Sham OVX treatment groups. Interdigitated bone volume fraction (BV/TV) increased with time for Sham OVX (0.022 BV/TV/wk) and OVX (0.015 BV/TV/wk) group, but the rate of increase was greater for the Sham OVX group (p = 0.0064). Tissue mineral density followed a similar increase with time in the interdigitated regions. Trabecular resorption, when it did occur, started at the cement border with medullary‐adjacent bone in the presence of osteoclasts. There was substantial loss of viable bone (~80% empty osteocyte lacunae) in the interdigitated regions. Pre‐surgical fluorochrome labels remained in the interdigitated regions, and did not diminish with time, indicating that the bone was not remodeling. There was also some evidence of continued surface mineralization in the interdigitated region after cementing of the knee, but this diminished over time. Statement of clinical significance: Interdigitated bone with cement provides mechanical stability for success of knee replacements. Improved understanding of the fate of the interdigitated bone over time could lead to a better understanding of the loosening process and interventions to prevent loss of fixation. © 2019 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 37:2163–2171, 2019

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Early Changes in Cement–Bone Fixation Using a Novel Rat Knee Replacement Model

Mann

Miller

Amendola

et al. 2019

Journal Orthopaedic Research

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“…So far, HR-pQCT imaging has only rarely been used to study bones of marine mammals [46, 47]. A number of previous studies [16–18, 20,21] used dual-energy X-ray absorptiometry (DXA), a method providing aBMD data [48].…”

Section: Discussionmentioning

confidence: 99%

Age-related changes in size, bone microarchitecture and volumetric bone mineral density of the mandible in the harbor seal (Phoca vitulina)

et al. 2019

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Detailed knowledge of age-related changes in the structure and mineralization of bones is important for interpreting osseous changes in wild mammals caused by exposure to environmental contaminants. This study analyzed mandibular size, microarchitecture and volumetric bone mineral density (vBMD) in harbor seals (n = 93, age range 0.5 months to 25 years) from the German North Sea. Bone microarchitecture and vBMD were assessed using high-resolution peripheral quantitative computed tomography (HR-pQCT). Significant differences were observed between the analyzed age classes (i) young juveniles (0.5–10 months), (ii) yearlings (12–23 months), and (iii) adults (12–25 years) for several of the variables, indicating an overall increase in cortical and trabecular area, cortical thickness and total and cortical vBMD with age. Furthermore, for juvenile animals (≤ 23 months), significant positive correlations with age were observed for mandible length and perimeter, cortical area, cortical thickness, trabecular separation, and total and cortical vBMD. The findings demonstrate a rapid increase in overall size, cortical dimensions and the degree of mineralization of the harbor seal mandible during the first two years after birth. Negative correlations with age existed for trabecular number and thickness as well as for trabecular bone volume fraction in the juveniles. The findings suggest a reduction in trabecular bone volume fraction with age, due to the bone trabeculae becoming thinner, less numerous and more widely spaced. Given the strong age dependence of most analyzed parameters, it is recommended to standardize samples with respect to age in future studies comparing microarchitecture and mineralization of harbor seal mandibles from different populations or different collection periods.

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“…For example, the mineral content of this bone in fin whale (Balaenoptera physalus) was measured as 86.4% [19]. In spite of few publications concerning its structure [20], morphology [21][22][23][24][25] including application of the modern microcomputed tomography (µ-CT) [25][26][27], and histology [28,29] most scientific attention has been focused on the materials properties [19] as well as functional role of this highly specialized bone in ultrasonic hearing and echolocation of whales [30][31][32][33][34][35][36].The large relative and absolute sizes of the ear bones of the sperm whale embryos (as well as the baleen whales) are striking. For example, in a 73-mm long embryo, the ear bone had a size of 27 mm, and in the prenatal (365 cm long) it already reached the size of the ear bone of an adult animal, which can be explained, apparently, by the same functional load on the hearing organ in newborns and adult whales.…”

Section: Introductionmentioning

confidence: 99%

“…According to the modern hypothesis, "ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing" [27]. However, the principles of calcification and the development of such hypermineralized bones as tympanic bulla of whales as well as the corresponding chemical driving forces that pattern the architecture of such unique biominerals remains unknown.…”

Section: Introductionmentioning

confidence: 99%

Extreme biomineralization: the case of the hypermineralized ear bone of gray whale (Eschrichtius robustus)

et al. 2020

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Selected hypermineralized bones (rostrum and tympanic bullae) have yet to be characterized for diverse species of whales (Cetacea). Hypermineralization in these structures is an example of extreme biomineralization that, however, occurs at temperatures around 36 °C. In this study we present the results of analytical investigations of the specimen of tympanic bulla isolated from gray whale (Eschrichtius robustus) for the first time. Examination of the internal surface of the bone mechanically crushed under a press revealed the presence of a lipid-containing phase, which did not disappear even after complete demineralization of the bone material. Additionally, analytical investigations including CARS, ATR-FTIR, Raman and XRD confirmed the presence of carbonated bioapatite and a collagen- lipid complex as the main components of this up to 2.34 kg/cm3 dense bone. Our experimental results open the way for further research on understanding of the principles of hypermineralization in highly specialized whale bones.

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Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing

Abstract: Cite this article: Schmidt FN et al. 2018 Ultra-high matrix mineralization of sperm whale auditory ossicles facilitates high sound pressure and high-frequency underwater hearing. Proc. R. Soc. B 285: 20181820. http://dx.

Cited by 17 publications

References 32 publications

Early Changes in Cement–Bone Fixation Using a Novel Rat Knee Replacement Model

Early Changes in Cement–Bone Fixation Using a Novel Rat Knee Replacement Model

Age-related changes in size, bone microarchitecture and volumetric bone mineral density of the mandible in the harbor seal (Phoca vitulina)

Extreme biomineralization: the case of the hypermineralized ear bone of gray whale (Eschrichtius robustus)

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