Axially loaded whole teeth of Atlantic wolffish exhibit negative Poisson’s ratios due to their osteodentin microarchitecture
Source abstract
Abstract
The Atlantic wolffish (Anarhichas lupus) is a teleost with prominent teeth highly adapted for crushing hard-shelled prey. The dentin type of wolffish teeth is osteodentin, which differs markedly in structure from the dentin of most vertebrates. This study aimed to investigate the three-dimensional (3D) deformation and strain fields that develop in intact wolffish teeth under load. Eight wolffish teeth (three caniniform and five molariform) were studied using low- and high-energy phase-contrast-enhanced x-ray tomography, imaged both statically and during in situ compression loading. Digital volume correlation was applied to sets of unloaded and loaded scans. Unexpectedly, 3D deformations and strains showed that all teeth exhibited auxeticity (negative Poisson's ratios), such that when a tooth is compressed longitudinally, it also contracts laterally. Strain fields were used to calculate effective Poisson's ratios in the x-z and y-z orientations (with z as the loading direction), and yielded negative values, mostly between -1 and -2. Auxeticity is rare in mineralized biomaterials and has previously been reported only in two invertebrates (limpet teeth and nacre). Nanoindentation showed that the solid osteodentinal components have bone-like mechanical properties. Microstructural analysis of osteodentin revealed a mineralized matrix with a vast array of canals that mostly run straight up from the base, and curve outward as they approach the tooth tip. We suggest that the internal architecture of osteodentin may explain its auxeticity through a mechanism similar to that of re-entrant auxetic metamaterials. Specifically, the externally curved canals and the mineralized columns between them bend inward under compression. STATEMENT OF SIGNIFICANCE: Here we report the surprising findings of negative Poisson's ratios (auxeticity) in osteodentin of wolffish (Anarhichas lupus) teeth. This means that when these teeth are compressed along their length, their width also contracts. This is a rare phenomenon which has not been reported so far in mineralized tissues of vertebrates. We propose that the cause of this unusual property is the internal micro-architecture of osteodentin, particularly its vast array of canals. Since materials with this property exhibit superior mechanical properties, such as resistance to wear and impact, this finding may lead to the development of new synthetic biomaterials with desirable features.
Source: openalex_inverted_index · Quality: baseline
Research context
OpenAlex topics: Calcium Carbonate Crystallization and Inhibition · Bone Tissue Engineering Materials · Cellular and Composite Structures
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References (93)
Show source-provided references
1. Origin and evolution of bone and dentin, and of their phosphorylated, acid-rich matrix proteins
2. Learning from evolutionary optimisation: what are toughening mechanisms good for in dentine, a nonrepairing bone tissue?10.1088/1748-3190/11/5/051003 ↗
3. Vertebrate mineralized tissues: a modular structural analysis10.1016/j.actbio.2024.03.026 ↗
4. NIH Public Access
5. B. Berkovitz, P. Shellis, The teeth of non-mammalian vertebrates, (2017) 311–330. https://doi.org/10.1016/b978-0-12-802850-6.00012-6.10.1016/B978-0-12-802850-6.00012-6 ↗
6. A. Nanci, Ten Cate’s Oral histology, (2013) ix. https://doi.org/10.1016/b978-0-323-07846-7.00021-5.10.1016/B978-0-323-07846-7.00021-5 ↗
7. Insights into whole bone and tooth function using optical metrology10.1007/s10853-007-1693-8 ↗
8. Compressive residual strains in mineral nanoparticles as a possible origin of enhanced crack resistance in Human tooth dentin10.1021/acs.nanolett.5b00143 ↗
9. Structure and mechanical properties of the soft zone separating bulk dentin and enamel in crowns of human teeth: insight into tooth function10.1016/j.jsb.2005.10.010 ↗
10. Water-mediated collagen and mineral nanoparticle interactions guide functional deformation of Human tooth dentin10.1021/acs.chemmater.6b00811 ↗
11. X-ray diffraction and in situ pressurization of dentine apatite reveals nanocrystal modulus stiffening upon carbonate removal10.1016/j.actbio.2020.09.004 ↗
12. Crack blunting, crack bridging and resistance-curve fracture mechanics in dentin: effect of hydration10.1016/S0142-9612(03)00458-7 ↗
13. Continuous tooth replacement: what can teleost fish teach us?10.1111/brv.13045 ↗
14. Comparative histology of caniniform teeth in some predatory ichthyophagous teleosts
15. Palaeohistological notes: 4 the interpretation of osteodentine, with remarks on the dentition in the devonian dipnoan Griphognathus10.1111/j.1463-6409.1976.tb00684.x ↗
16. Evolution of patterns and processes in teeth and tooth-related tissues in non-mammalian vertebrates10.1111/j.1600-0722.1998.tb02211.x ↗
17. Insights into the structure and composition of the peritubular dentin organic matrix and the lamina limitans10.1016/j.micron.2011.08.003 ↗
18. Ultrastructural examination of dentin using focused ion-beam cross-sectioning and transmission electron microscopy10.1016/j.micron.2005.05.011 ↗
19. Focused ion beam-SEM 3D study of osteodentin in the teeth of the Atlantic wolfish Anarhichas lupus10.1016/j.jsb.2024.108062 ↗
20. Osteodentin in the Atlantic wolffish (Anarhichas lupus): dentin or bone?
21. Intraspecific variation in feeding mechanics and bite force in durophagous stingrays10.1111/jzo.12530 ↗
22. Functional and developmental morphology of tooth replacement in the Atlantic Wolffish, Anarhichas lupus (Teleostei: Zoarcoidei: Anarhichadidae)10.1643/OT-14-141 ↗
23. Bite force and performance in the durophagous bonnethead shark, Sphyrna tiburo
24. Comparative analysis of methods for determining bite force in the spiny dogfish Squalus acanthias
25. F. Faizan, Atlantic Wolffish, (2024). https://oceaninfo.com/animals/atlantic-wolffish/ (accessed 2024).
26. Nano- and micromechanical properties of dentine: investigation of differences with tooth side10.1016/j.jbiomech.2011.03.004 ↗
27. A micromechanics model of the elastic properties of human dentine10.1016/S0003-9969(99)00080-1 ↗
28. Nanoscopic dynamic mechanical properties of intertubular and peritubular dentin10.1016/j.jmbbm.2011.08.010 ↗
29. Relations between shape, materials properties, and function in biological materials using laser speckle interferometry: in situ tooth deformation10.1002/adfm.200600120 ↗
30. Young’s modulus of peritubular and intertubular human dentin by nano-indentation tests10.1016/j.jsb.2010.09.010 ↗
31. A composite resin core with a new zirconia tube reduces the surface strain at the cervical area of a mandibular molar: a model tooth study10.2186/jpr.JPR_D_21_00243 ↗
32. Effect of cavity design on tooth surface strain10.1016/j.prosdent.2013.08.004 ↗
33. Digital image correlation and strain gauges to map and compare strain in teeth with different quantity and quality of remaining tooth structure10.11607/ijp.6044 ↗
34. Human root dentin: structural anisotropy and vickers microhardness isotropy10.3109/03008209809021502 ↗
35. Enamel dictates whole tooth deformation: a finite element model study validated by a metrology method10.1016/j.jsb.2009.07.019 ↗
36. Determining the elastic modulus of mouse cortical bone using electronic speckle pattern interferometry (ESPI) and micro computed tomography: a new approach for characterizing small-bone material properties10.1016/j.bone.2009.03.664 ↗
37. Stress–strain response in human dentine: rethinking fracture predilection in postcore restored teeth10.1111/j.1600-4469.2004.00250.x ↗
38. Importance of the variable periodontal ligament geometry for whole tooth mechanical function_ A validated numerical study
39. Strain patterns in cervical enamel of teeth subjected to occlusal loading10.1016/S0109-5641(00)00036-1 ↗
40. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object10.1046/j.1365-2818.2002.01010.x ↗
41. TomoPress—In situ synchrotron-based microtomography under axial load10.3390/instruments4020011 ↗
42. Uncertainties of synchrotron microCT-based digital volume correlation bone strain measurements under simulated deformation10.1016/j.jbiomech.2019.01.041 ↗
43. High resolution synchrotron-based radiography and tomography using hard X-rays at the BAMline (BESSY II)10.1016/j.nima.2007.11.020 ↗
44. An improved technique for determining hardness and elastic-modulus using load and displacement sensing indentation experiments10.1557/JMR.1992.1564 ↗
45. A novel auxetic 3D lattice structure for enhancing energy absorption10.1016/j.compstruct.2023.117620 ↗
46. Indentation resistance of brittle auxetic structures: combining discrete representation and continuum model10.1016/j.engfracmech.2021.107824 ↗
47. Kolken · 2017 · 5111
48. Digital volume correlation: three-dimensional strain mapping using X-ray tomography10.1007/BF02323555 ↗
49. 3D analysis from micro-MRI during in situ compression on cancellous bone10.1016/j.jbiomech.2009.06.034 ↗
50. Glenoid bone strain after anatomical total shoulder arthroplasty: in vitro measurements with micro-CT and digital volume correlation10.1016/j.medengphy.2020.09.009 ↗
51. High resolution three-dimensional strain measurements in human articular cartilage10.1016/j.jmbbm.2021.104806 ↗
52. Digital volume correlation for the characterization of musculoskeletal tissues: current challenges and future developments10.3389/fbioe.2022.1010056 ↗
53. Synchrotron tomography of intervertebral disc deformation quantified by digital volume correlation reveals microstructural influence on strain patterns10.1016/j.actbio.2019.05.021 ↗
54. Micromechanical evaluation of cortical bone using in situ XCT indentation and digital volume correlation10.1016/j.jmbbm.2020.104298 ↗
55. The application of digital volume correlation (DVC) to evaluate strain predictions generated by finite element models of the osteoarthritic humeral head10.1007/s10439-020-02549-2 ↗
56. In situ characterization of nanoscale strains in loaded whole joints via synchrotron X-ray tomography10.1038/s41551-019-0477-1 ↗
57. A novel approach to evaluate the effects of artificial bone focal lesion on the three-dimensional strain distributions within the vertebral body10.1371/journal.pone.0251873 ↗
58. 3D full-field biomechanical testing of a glenoid before and after implant placement10.1016/j.eml.2019.100614 ↗
59. Nacre-inspired auxetic interlocking brick-and-mortar composites10.1016/j.coco.2024.101892 ↗
60. Large deformation and energy absorption of additively manufactured auxetic materials and structures: a review10.1016/j.compositesb.2020.108340 ↗
61. Shape-morphing metamaterials
62. Negative Poisson’s ratio in modern functional materials10.1002/adma.201601363 ↗
63. mechanical properties of additively manufactured thick honeycombs10.3390/ma9080613 ↗
64. 3D Soft metamaterials with negative poisson’s ratio10.1002/adma.201301986 ↗
65. Negative Poisson’s ratios in tendons: an unexpected mechanical response10.1016/j.actbio.2015.06.018 ↗
66. Poisson’s ratio in skin
67. Non-invasive determination of the complete elastic moduli of spider silks10.1038/nmat3549 ↗
68. Lower hardness than strength: the auxetic composite microstructure of limpet tooth10.1016/j.actbio.2023.04.035 ↗
69. Limpet teeth microstructure unites auxeticity with extreme strength and high stiffness10.1126/sciadv.add4644 ↗
70. Effect of a negative poisson ratio in the tension of ceramics10.1103/PhysRevLett.100.245502 ↗
71. Properties and an anisotropic model of cancellous bone from the proximal tibial epiphysis10.1115/1.3138303 ↗
72. A pavement of pearl10.1038/40010 ↗
73. Mechanical properties of mother of pearl in tension
74. Poisson’s ratio and modern materials10.1038/nmat3134 ↗
75. Foam structures with a negative poisson’s ratio10.1126/science.235.4792.1038 ↗
76. Poisson’s ratio for anisotropic elastic materials can have no bounds10.1093/qjmamj/hbh021 ↗
77. Mechanical basis of bone strength: influence of bone material, bone structure and muscle action
78. Importance of age on the dynamic mechanical behavior of intertubular and peritubular dentin10.1016/j.jmbbm.2014.11.021 ↗
79. Shape-preserving erosion controlled by the graded microarchitecture of shark tooth enameloid10.1038/s41467-020-19739-0 ↗
80. Predation versus protection: fish teeth and scales evaluated by nanoindentation10.1557/jmr.2011.332 ↗
81. Structure, property, and function of sheepshead (Archosargus probatocephalus) teeth10.1016/j.archoralbio.2018.01.013 ↗
82. Mechanics of pharyngeal teeth of black carp ( Mylopharyngodon piceus) crushing mollusk shells10.1002/adem.201200304 ↗
83. 3D relationship between hierarchical canal network and gradient mineralization of shark tooth osteodentin
84. Printing Nature_ unraveling the role of Nacre’s mineral bridges
85. Young’s modulus and hardness of shark tooth biomaterials10.1016/j.archoralbio.2010.01.001 ↗
86. The dentin substrate: structure and properties related to bonding10.1016/S0300-5712(96)00065-6 ↗
87. The material bone: structure-mechanical function relations10.1146/annurev.matsci.28.1.271 ↗
88. Chemical composition and structure of peritubular and intertubular human dentine revisited10.1016/j.archoralbio.2011.09.008 ↗
89. The effect of microcracking in the peritubular dentin on the fracture of dentin10.1016/j.jbiomech.2017.10.022 ↗
90. A design method for metamaterials: 3D transversely isotropic lattice structures with tunable auxeticity10.1088/1361-665X/ac411f ↗
91. Measurement of thermophysical properties of human dentin: effect of open porosity10.1016/j.jdent.2008.04.006 ↗
92. Cavities in the compact bone in tetrapods and fish and their effect on mechanical properties10.1016/j.jsb.2013.04.012 ↗
93. Estimation of bone matrix apparent stiffness variation caused by osteocyte lacunar size and density10.1115/1.1338123 ↗