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Research Article

Nanostructural origins of irreversible deformation in bone revealed by an in situ atomic force microscopy study

Tianbao Qian1,2,4,5,6,7, Lijing Teng1, Yongji Zhou1, Minghao Zhang3,4,5,6,7, Zuquan Hu1( ), Xiaofeng Chen3,4,5,6,7( ), Fei Hang3,4,5,6,7( )
School of Biology & Engineering, Guizhou Medical University, Guiyang 550025, China
School of Medicine, South China University of Technology, Guangzhou 510006, China
School of Materials Science and Engineering, South China University of Technology, Guangzhou 510641, China
National Engineering Research Center for Tissue Restoration and Reconstruction, South China University of Technology, Guangzhou 510006, China
Key Laboratory of Biomedical Engineering of Guangdong Province, South China University of Technology, Guangzhou 510006, China
Key Laboratory of Biomedical Materials and Engineering of the Ministry of Education, South China University of Technology, Guangzhou 510006, China
Innovation Center for Tissue Restoration and Reconstruction, South China University of Technology, Guangzhou 510006, China
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Graphical Abstract

The nanoscale plastic deformation process in bone includes the first stage (slipping between fibril arrays) characterized by mineral aggregate grains, and the second stage (interfibrillar slipping) with the feature of the exposed mineralized collagen fibrils.

Abstract

The structural origins of bone toughness at the nanoscale are not completely understood. Therefore, we performed in situ scanning using atomic force microscopy during macroscopic mechanical testing of antler and bovine bone, to reveal the origins of the irreversible plastic deformation at the mineralized collagen fibril (MCF) array and MCF levels. We found that the plastic deformation behavior at the nanoscale level could be divided into two stages. The first stage of plastic deformation at the nanoscale level was characterized by slippage between the MCF arrays, which contained mineral aggregate grains with regular shapes under load. In the second stage of nanoscale plastic deformation, the MCFs broke through the bonds of the extrafibrillar mineral aggregate grains and exhibited interfibrillar slippage. These nanoscale plastic deformation behaviors may thus be the origins of stress whitening and irreversible plastic deformation. Thus, the findings in this study not only shed light on the plastic deformation mechanisms of MCF arrays and MCFs, but also provide structural and mechanistic insights into bioinspired materials design and mechanisms of relevant bone diseases.

Keywords

cortical boneatomic force microscopyplastic deformationmineralized collagen fibrilinterfibrillar slipping

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References

1

Ritchie, R. O.; Buehler, M. J.; Hansma, P. Plasticity and toughness in bone. Phys. Today 2009, 62, 41–47.
Google Scholar
2

Morsali, R.; Dai, Z. W.; Wang, Y.; Qian, D.; Minary-Jolandan, M. Deformation mechanisms of “two-part” natural adhesive in bone interfibrillar nano-interfaces. ACS Biomater. Sci. Eng. 2019, 5, 5916–5924.
Crossref Google Scholar
3

Nyman, J. S.; Roy, A.; Reyes, M. J.; Wang, X. D. Mechanical behavior of human cortical bone in cycles of advancing tensile strain for two age groups. J. Biomed. Mater. Res. Part A 2009, 89A, 521–529.
Crossref Google Scholar
4

Nyman, J. S.; Leng, H. J.; Dong, X. N.; Wang, X. D. Differences in the mechanical behavior of cortical bone between compression and tension when subjected to progressive loading. J. Mech. Behav. Biomed. Mater. 2009, 2, 613–619.
Crossref Google Scholar
5

Wang, X. D.; Nyman, J. S. A novel approach to assess post-yield energy dissipation of bone in tension. J. Biomech. 2007, 40, 674–677.
Crossref Google Scholar
6

Nyman, J. S.; Roy, A.; Tyler, J. H.; Acuna, R. L.; Gayle, H. J.; Wang, X. D. Age-related factors affecting the postyield energy dissipation of human cortical bone. J. Orthop. Res. 2007, 25, 646–655.
Crossref Google Scholar
7

De Falco, P.; Barbieri, E.; Pugno, N.; Gupta, H. S. Staggered fibrils and damageable interfaces lead concurrently and independently to hysteretic energy absorption and inhomogeneous strain fields in cyclically loaded antler bone. ACS Biomater. Sci. Eng. 2017, 3, 2779–2787.
Crossref Google Scholar
8

Nalla, R. K.; Kinney, J. H.; Ritchie, R. O. Mechanistic fracture criteria for the failure of human cortical bone. Nat. Mater. 2003, 2, 164–168.
Crossref Google Scholar
9

Vashishth, D.; Behiri, J. C.; Bonfield, W. Crack growth resistance in cortical bone: Concept of microcrack toughening. J. Biomech. 1997, 30, 763–769.
Crossref Google Scholar
10

Vashishth, D.; Tanner, K. E.; Bonfield, W. Experimental validation of a microcracking-based toughening mechanism for cortical bone. J. Biomech. 2003, 36, 121–124.
Crossref Google Scholar
11

Gupta, H. S.; Krauss, S.; Kerschnitzki, M.; Karunaratne, A.; Dunlop, J. W. C.; Barber, A. H.; Boesecke, P.; Funari, S. S.; Fratzl, P. Intrafibrillar plasticity through mineral/collagen sliding is the dominant mechanism for the extreme toughness of antler bone. J. Mech. Behav. Biomed. Mater. 2013, 28, 366–382.
Crossref Google Scholar
12

Krauss, S.; Fratzl, P.; Seto, J.; Currey, J. D.; Estevez, J. A.; Funari, S. S.; Gupta, H. S. Inhomogeneous fibril stretching in antler starts after macroscopic yielding: Indication for a nanoscale toughening mechanism. Bone 2009, 44, 1105–1110.
Crossref Google Scholar
13

Weiner, S.; Wagner, H. D. The material bone: Structure-mechanical function relations. Annu. Rev. Mater. Sci. 1998, 28, 271–298.
Crossref Google Scholar
14

Tai, K.; Ulm, F. J.; Ortiz, C. Nanogranular origins of the strength of bone. Nano Lett. 2006, 6, 2520–2525.
Crossref Google Scholar
15

Hang, F.; Barber, A. H. Nano-mechanical properties of individual mineralized collagen fibrils from bone tissue. J. Roy. Soc. Interface 2010, 8, 500–505.
Google Scholar
16

Buehler, M. J. Molecular nanomechanics of nascent bone: Fibrillar toughening by mineralization. Nanotechnology 2007, 18, 295102.
Crossref Google Scholar
17

Gupta, H. S.; Wagermaier, W.; Zickler, G. A.; Aroush, D. R. B.; Funari, S. S.; Roschger, P.; Wagner, H. D.; Fratzl, P. Nanoscale deformation mechanisms in bone. Nano Lett. 2005, 5, 2108–2111.
Crossref Google Scholar
18

Gupta, H. S.; Seto, J.; Wagermaier, W.; Zaslansky, P.; Boesecke, P.; Fratzl, P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc. Natl. Acad. Sci. USA 2006, 103, 17741–17746.
Crossref Google Scholar
19

Lin, L. Q.; Samuel, J.; Zeng, X. W.; Wang, X. D. Contribution of extrafibrillar matrix to the mechanical behavior of bone using a novel cohesive finite element model. J. Mech. Behav. Biomed. Mater. 2017, 65, 224–235.
Crossref Google Scholar
20

Groetsch, A.; Gourrier, A.; Schwiedrzik, J.; Sztucki, M.; Beck, R. J.; Shephard, J. D.; Michler, J.; Zysset, P. K.; Wolfram, U. Compressive behaviour of uniaxially aligned individual mineralised collagen fibres at the micro- and nanoscale. Acta Biomater. 2019, 89, 313–329.
Crossref Google Scholar
21

Katsamenis, O. L.; Chong, H. M. H.; Andriotis, O. G.; Thurner, P. J. Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level. J. Mech. Behav. Biomed. Mater. 2013, 17, 152–165.
Crossref Google Scholar
22

Maghsoudi-Ganjeh, M.; Samuel, J.; Ahsan, A. S.; Wang, X. D.; Zeng, X. W. Intrafibrillar mineralization deficiency and osteogenesis imperfecta mouse bone fragility. J. Mech. Behav. Biomed. Mater. 2021, 117, 104377.
Crossref Google Scholar
23

Wang, Y. H.; Ural, A. Mineralized collagen fibril network spatial arrangement influences cortical bone fracture behavior. J. Biomech. 2018, 66, 70–77.
Crossref Google Scholar
24

Wang, Y. H.; Ural, A. Effect of modifications in mineralized collagen fibril and extra-fibrillar matrix material properties on submicroscale mechanical behavior of cortical bone. J. Mech. Behav. Biomed. Mater. 2018, 82, 18–26.
Crossref Google Scholar
25

Wang, Y. H.; Ural, A. A three-dimensional multiscale finite element model of bone coupling mineralized collagen fibril networks and lamellae. J. Biomech. 2020, 112, 110041.
Crossref Google Scholar
26

Wang, Y.; Ural, A. A finite element study evaluating the influence of mineralization distribution and content on the tensile mechanical response of mineralized collagen fibril networks. J. Mech. Behav. Biomed. Mater. 2019, 100, 103361.
Crossref Google Scholar
27

Fang, M.; Goldstein, E. L.; Turner, A. S.; Les, C. M.; Orr, B. G.; Fisher, G. J.; Welch, K. B.; Rothman, E. D.; Holl, M. M. B. Type I collagen D-spacing in fibril bundles of dermis, tendon, and bone: Bridging between nano- and micro-level tissue hierarchy. ACS Nano 2012, 6, 9503–9514.
Crossref Google Scholar
28

Zhao, H. X.; Jin, H.; Cai, J. Y.; Ding, S. The process of collagen biomineralization observed by AFM in a model dual membrane diffusion system. Ultramicroscopy 2010, 110, 1306–1311.
Crossref Google Scholar
29

Balooch, M.; Habelitz, S.; Kinney, J. H.; Marshall, S. J.; Marshall, G. W. Mechanical properties of mineralized collagen fibrils as influenced by demineralization. J. Struct. Biol. 2008, 162, 404–410.
Crossref Google Scholar
30

Xu, Z. H.; Li, X. D. Deformation strengthening of biopolymer in nacre. Adv. Funct. Mater. 2011, 21, 3883–3888.
Crossref Google Scholar
31

Grégoire, D.; Loh, O.; Juster, A.; Espinosa, H. D. In-situ AFM experiments with discontinuous DIC applied to damage identification in biomaterials. Exp. Mech. 2011, 51, 591–607.
Crossref Google Scholar
32

Seshadri, I. P.; Bhushan, B. In situ tensile deformation characterization of human hair with atomic force microscopy. Acta Mater. 2008, 56, 774–781.
Crossref Google Scholar
33

Lin, Z. X.; Xu, Z. H.; An, Y. H.; Li, X. D. In situ observation of fracture behavior of canine cortical bone under bending. Mater. Sci. Eng.: C 2016, 62, 361–367.
Crossref Google Scholar
34

Qian, T. B.; Chen, X. X.; Hang, F.; Zhuang, J.; Chen, X. F. Ordered fibril arrays in osteons promote the multidirectional nanodeflection of cracks: In situ AFM imaging. ACS Biomater. Sci. Eng. 2021, 7, 2372–2382.
Crossref Google Scholar
35

Chen, X. X.; Qian, T. B.; Hang, F.; Chen, X. F. Water promotes the formation of fibril bridging in antler bone illuminated by in situ AFM testing. J. Mech. Behav. Biomed. Mater. 2021, 120, 104580.
Crossref Google Scholar
36

Qian, T. B.; Chen, X. X.; Hang, F. Investigation of nanoscale failure behaviour of cortical bone under stress by AFM. J. Mech. Behav. Biomed. Mater. 2020, 112, 103989.
Crossref Google Scholar
37

Shen, L.; Liu, T. X.; Lv, P. F. Polishing effect on nanoindentation behavior of nylon 66 and its nanocomposites. Polym. Test. 2005, 24, 746–749.
Crossref Google Scholar
38

Zioupos, P.; Wang, X. T.; Currey, J. D. Experimental and theoretical quantification of the development of damage in fatigue tests of bone and antler. J. Biomech. 1996, 29, 989–1002.
Crossref Google Scholar
39

Currey, J. D.; Landete-Castillejos, T.; Estevez, J.; Ceacero, F.; Olguin, A.; Garcia, A.; Gallego, L. The mechanical properties of red deer antler bone when used in fighting. J. Exp. Biol. 2009, 212, 3985–3993.
Crossref Google Scholar
40

Hardisty, M. R.; Garcia, T. C.; Choy, S.; Dahmubed, J.; Stover, S. M.; Fyhrie, D. P. Stress-whitening occurs in demineralized bone. Bone 2013, 57, 367–374.
Crossref Google Scholar
41
Currey, J. D. Bones: Structure and Mechanics; Princeton University Press: Princeton, 2002.
42

Sun, X. B.; Hoon Jeon, J.; Blendell, J.; Akkus, O. Visualization of a phantom post-yield deformation process in cortical bone. J. Biomech. 2010, 43, 1989–1996.
Crossref Google Scholar
43

Reznikov, N.; Bilton, M.; Lari, L.; Stevens, M. M.; Kröger, R. Fractal-like hierarchical organization of bone begins at the nanoscale. Science 2018, 360, eaao2189.
Crossref Google Scholar
44

Zhou, C.; Zhang, X. L.; Ai, J.; Ji, T.; Nagai, M.; Duan, Y. Y.; Che, S. A.; Han, L. Chiral hierarchical structure of bone minerals. Nano Res. 2022, 15, 1295–1302.
Crossref Google Scholar
45

McNally, E. A.; Schwarcz, H. P.; Botton, G. A.; Arsenault, A. L. A model for the ultrastructure of bone based on electron microscopy of ion-milled sections. PLoS One 2012, 7, e29258.
Crossref Google Scholar
46

Gao, H. J. Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. Int. J. Fracture 2006, 138, 101.
Crossref Google Scholar
47

Stock, S. R. The mineral–collagen interface in bone. Calcif. Tissue Int. 2015, 97, 262–280.
Crossref Google Scholar
48

Fratzl, P.; Kolednik, O.; Fischer, F. D.; Dean, M. N. The mechanics of tessellations-bioinspired strategies for fracture resistance. Chem. Soc. Rev. 2016, 45, 252–267.
Crossref Google Scholar
49

Weiner, S.; Price, P. A. Disaggregation of bone into crystals. Calcif. Tissue Int. 1986, 39, 365–375.
Crossref Google Scholar
50

Qin, Z.; Gautieri, A.; Nair, A. K.; Inbar, H.; Buehler, M. J. Thickness of hydroxyapatite nanocrystal controls mechanical properties of the collagen–hydroxyapatite interface. Langmuir 2012, 28, 1982–1992.
Crossref Google Scholar
Nano Research
Volume 15 Issue 8,
August 2022
Pages 7329-7341
DOI: 10.1007/s12274-022-4365-8
Cite this article:
Qian T, Teng L, Zhou Y, et al. Nanostructural origins of irreversible deformation in bone revealed by an in situ atomic force microscopy study. Nano Research, 2022, 15(8): 7329-7341. https://doi.org/10.1007/s12274-022-4365-8
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Received: 28 December 2021
Revised: 27 March 2022
Accepted: 28 March 2022
Published: 31 May 2022
© Tsinghua University Press 2022
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