journal article·2022-06

How suture networks improve the protective function of natural structures: A multiscale investigation

B Alheit, S Bargmann, BD Reddy

Acta Biomaterialia· Volume 145
Publisher page

Abstract

Myriad natural protective structures consist of bone plates joined by convoluted unmineralized (soft) collagenous sutures. Examples of such protective structures include: shells of turtles, craniums of almost all animals (including humans), alligator armour, armadillo armour, and others. The function of sutures has been well researched. However, whether, and if so how, sutures improve protective performance during a predator attack has received limited attention. Sutures are ubiquitous in protective structures, and this motivates the question as to whether sutures optimize the protective function of the structure. Hence, in this work the behaviour of structures that contain sutures during predator attacks is investigated. We show that sutures decrease the maximum strain energy density that turtle shells experience during predator attacks by more than an order of magnitude. Hence, sutures make turtle shells far more resilient to material failure, such as, fracture, damage, and plastic deformations. Additionally, sutures increase the viscous behaviour of the shell causing increased dissipation of energy during predator attacks. Further investigations into the influence of sutures on behaviour during locomotion and breathing are also presented. The results presented in this work motivate the inclusion of sutures in biomimetically designed protective structures, such as helmets and protective clothing. STATEMENT OF SIGNIFICANCE: Myriad bony protective structures contain networks of sutures, that is con- voluted soft collagenous tissue. Their ubiquity motivates the question, whether, and if so how, sutures improve protective performance. Hence, this work inves- tigates how sutures affect protective performance using computational experi- ments. Due to the length scale of sutures being far smaller than the structures in which they reside, classical modelling approaches are prohibitively expensive. Hence, in this work, a multiscale approach is taken. To our knowledge, this is the first multiscale investigation of structures that contain sutures. Among other insights, we show that sutures decrease the maximum strain energy density in structures during predator attacks by over an order of mag- nitude. Hence, sutures make structures far more resilient to failure.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Cellular Mechanics and Interactions · Elasticity and Material Modeling · Bone Tissue Engineering Materials

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (57)

Show source-provided references
1. S. Fraberger, M. Dockner, E. Winter, M. Pretterklieber, G. W. Weber, M. Teschler-Nicola, P. Pietschmann, Micro-ct evaluation of historical human skulls presenting signs of syphilitic infection, 2021, (License: https://creativecommons.org/licenses/by/4.0/).10.1007/s00508-021-01832-z ↗
2. Black caiman skeleton, 2012, (License: https://creativecommons.org/licenses/by-sa/2.0/).
3. Mechanical function of a complex three-dimensional suture joining the bony elements in the shell of the red-eared slider turtle10.1002/adma.200801256 ↗
4. Animal models of cranial suture biology
5. Finite element analysis of impact and shaking inflicted to a child10.1007/s00414-006-0129-3 ↗
6. Structural design and mechanical behavior of alligator (alligator mississippiensis) osteoderms10.1016/j.actbio.2013.07.016 ↗
7. Armadillo armor: mechanical testing and micro-structural evaluation10.1016/j.jmbbm.2010.12.013 ↗
8. Structure and fracture resistance of alligator gar (atractosteus spatula) armored fish scales10.1016/j.actbio.2012.12.026 ↗
9. Assessment of the role of sutures in a lizard skull: a computer modelling study10.1098/rspb.2008.0863 ↗
10. The global impact of sutures assessed in a finite element model of a macaque cranium10.1002/ar.21203 ↗
11. Mechanical properties of cranial sutures10.1016/0021-9290(90)90059-C ↗
12. Evolution of complexity in paleozoic ammonoid sutures10.1126/science.286.5440.760 ↗
13. Darwin · 2016
14. Divergent evolution through cumulative segregation10.1111/j.1096-3642.1888.tb01445.x ↗
15. Mechanics of cranial sutures during simulated cyclic loading10.1016/j.jbiomech.2012.05.007 ↗
16. Cranial sutures work collectively to distribute strain throughout the reptile skull10.1098/rsif.2013.0442 ↗
17. Cranial sutures as intramembranous bone growth sites10.1002/1097-0177(2000)9999:9999<::AID-DVDY1073>3.0.CO;2-F ↗
18. Dimensional, geometrical, and physical constraints in skull growth10.1103/PhysRevLett.118.248101 ↗
19. A mathematical model for mechanotransduction at the early steps of suture formation10.1098/rspb.2012.2670 ↗
20. Computationally modelling the mechanical behaviour of turtle shell sutures — a natural interlocking structure10.1016/j.jmbbm.2020.103973 ↗
21. Dynamic mechanical behaviour of suture interfaces as inspiration for architectured hierarchical interlocking composites10.1016/j.jmps.2021.104620 ↗
22. A multilevel finite element method (fe2) to describe the response of highly non-linear structures using generalized continua10.1016/S0045-7825(03)00348-7 ↗
23. Generation of 3D representative volume elements for heterogeneous materials: a review10.1016/j.pmatsci.2018.02.003 ↗
24. Elastic properties of reinforced solids: some theoretical principles10.1016/0022-5096(63)90036-X ↗
25. On constitutive macro-variables for heterogeneous solids at finite strain10.1098/rspa.1972.0001 ↗
26. Zohdi · 2004 · volume 20
27. Computational homogenization of nonlinear elastic materials using neural networks10.1002/nme.4953 ↗
28. On-the-fly adaptivity for nonlinear twoscale simulations using artificial neural networks and reduced order modeling10.3389/fmats.2019.00075 ↗
29. Accelerating multiscale finite element simulations of history-dependent materials using a recurrent neural network10.1016/j.cma.2019.112594 ↗
30. A deep material network for multiscale topology learning and accelerated nonlinear modeling of heterogeneous materials10.1016/j.cma.2018.09.020 ↗
31. Deep learning predicts path-dependent plasticity10.1073/pnas.1911815116 ↗
32. Micromechanics-based surrogate models for the response of composites: a critical comparison between a classical mesoscale constitutive model, hyper-reduction and neural networks10.1016/j.euromechsol.2020.103995 ↗
33. Exploring the 3d architectures of deep material network in data-driven multiscale mechanics10.1016/j.jmps.2019.03.004 ↗
34. A computationally tractable framework for nonlinear dynamic multiscale modeling of membrane woven fabrics10.1002/nme.6634 ↗
35. On-the-fly construction of surrogate constitutive models for concurrent multiscale mechanical analysis through probabilistic machine learning
36. Model-data-driven constitutive responses: application to a multiscale computational framework
37. Hyperelastic modelling of arterial layers with distributed collagen fibre orientations10.1098/rsif.2005.0073 ↗
38. Tensile testing of bone over a wide range of strain rates: effects of strain rate, microstructure and density10.1007/BF02477046 ↗
39. Characterisation of the dynamic compressive mechanical properties of cancellous bone from the human cervical spine10.1016/j.ijimpeng.2005.03.006 ↗
40. Additive manufacturing of honeybee-inspired microneedle for easy skin insertion and difficult removal10.1021/acsami.8b09563 ↗
41. The relationship between lung volume, respiratory drive and breathing pattern in the turtle, chrysemys picta10.1242/jeb.120.1.233 ↗
42. Maximum static inspiratory and expiratory pressures with different lung volumes10.1186/1475-925X-5-29 ↗
43. Water-content related alterations in macro and micro scale tendon biomechanics10.1038/s41598-019-44306-z ↗
44. Viscoelastic properties of bone as a function of water content10.1016/0021-9290(94)00130-V ↗
45. Mechanical properties of cranial sutures10.1016/0021-9290(90)90059-C ↗
46. A generalized mechanical model for suture interfaces of arbitrary geometry10.1016/j.jmps.2012.10.004 ↗
47. Bioinspired, mechanical, deterministic fractal model for hierarchical suture joints10.1103/PhysRevE.85.031901 ↗
48. Achieving outstanding damping performance through bio-inspired sutural tessellations10.1016/j.jmps.2020.104010 ↗
49. Stiffness and strength of suture joints in nature10.1103/PhysRevE.84.062904 ↗
50. Interfacial toughening effect of suture structures10.1016/j.actbio.2019.11.034 ↗
51. Mechanical model of bio-inspired composites with sutural tessellation10.1016/j.jmps.2018.09.015 ↗
52. Invariant formulation of hyperelastic transverse isotropy based on polyconvex free energy functions10.1016/S0020-7683(02)00458-4 ↗
53. Truesdell · 2004
54. Simo · 2006 · volume 7
55. Holzapfel · 2000
56. Friedman · 2017
57. Numerical approximation of tangent moduli for finite element implementations of nonlinear hyperelastic material models10.1115/1.2979872 ↗