AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

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

Tianbao Qian1,2,4,5,6,7Lijing Teng1Yongji Zhou1Minghao Zhang3,4,5,6,7Zuquan 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
Show Author Information

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.

Electronic Supplementary Material

Download File(s)
12274_2022_4365_MOESM1_ESM.pdf (3.2 MB)

References

1

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

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.

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.

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.

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.

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.

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.

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.

9

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

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.

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.

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.

13

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

14

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

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.

16

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

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.

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.

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.

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.

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.

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.

23

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

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.

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.

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.

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.

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.

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.

30

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

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.

32

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

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

46

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

47

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

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.

49

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

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.

Nano Research
Pages 7329-7341
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
Topics:

1281

Views

2

Crossref

2

Web of Science

2

Scopus

0

CSCD

Altmetrics

Received: 28 December 2021
Revised: 27 March 2022
Accepted: 28 March 2022
Published: 31 May 2022
© Tsinghua University Press 2022
Return