Abstract
The denaturation of collagen at the molecular level in bone and dentin can impact their structure and properties, leading to increased brittleness in pathological diseases such as osteogenesis imperfecta, dentinogenesis imperfecta, diabetes, and cancer. This study investigates the relationship between collagen denaturation and the macroscale resistance of bone and dentin. Through heat treatment at \(160{^{\circ }}\hbox {C}\) on bovine bone and human dentin, the effects of collagen denaturation on macroscale flexural strength, scanning electron microscopy, and transmission electron microscopy imaging of micro- and nanostructure were studied. The results show that collagen denaturation decreases the resistance of bone and dentin to fracture, even though collagen denaturation did not impact the mineral organization around and inside collagen fibrils. This is attributable to (1) a reduction in bone and dentin ability to deform (e.g., 40–75% decrease in strain to failure) and to resist fracture (e.g., 83–95% decrease in work to fracture) properties and (2) to a smoother crack path with less crack deflection around microstructural features. Reduction in deformation and toughness not only removed plastic deformation but also drastically decreased elastic deformation and elastic work to fracture in all tissues. However, the elastic modulus was only affected in radial-oriented bone samples where collagen fibrils are oriented perpendicularly to crack opening forces. This study highlights the crucial role of collagen molecule integrity and orientation in bone/dentin deformability and resistance.
Similar content being viewed by others
References
E.A. Zimmermann, R.O. Ritchie, Adv. Healthc. Mater. 4(9), 1287 (2015)
R.B. Martin, D.B. Burr, N.A. Sharkey, D.P. Fyhrie, R.B. Martin, D.B. Burr, N.A. Sharkey, D.P. Fyhrie, Skelet. Tissue Mech. 355 (2015)
A. Carriero, E.A. Zimmermann, A. Paluszny, S.Y. Tang, H. Bale, B. Busse, T. Alliston, G. Kazakia, R.O. Ritchie, S.J. Shefelbine, J. Bone Miner. Res. 29(6), 1392 (2014)
M. Biria, F.M. Abbas, S. Mozaffar, R. Ahmadi, Dental Res. J. 9(4) (2012)
M.A. Saghiri, B. Rahmani, M. Conte, D. Nath, O.A. Peters, S.M. Morgano, Eur. Endod. J. 7(2), 122 (2022)
L.B. Bondarenko, Avicenna J. Med. Biochem. 7(2), 64 (2019)
K.L. Reigle, G. Di Lullo, K.R. Turner, J.A. Last, I. Chervoneva, D.E. Birk, J.L. Funderburgh, E. Elrod, M.W. Germann, C. Surber et al. J. Cell. Biochem. 104(5), 1684 (2008)
L.S. Mirigian, E. Makareeva, H. Koistinen, O. Itkonen, T. Sorsa, U.-H. Stenman, T. Salo, S. Leikin, Arch. Biochem. Biophys. 535(2), 111 (2013)
M.E. Launey, M.J. Buehler, R.O. Ritchie, Annu. Rev. Mater. Res. 40, 25 (2010)
C. Acevedo, V.A. Stadelmann, D.P. Pioletti, T. Alliston, R.O. Ritchie, Nat. Biomed. Eng. 2(2), 62 (2018)
C. Acevedo, M. Sylvia, E. Schaible, J.L. Graham, K.L. Stanhope, L.N. Metz, B. Gludovatz, A.V. Schwartz, R.O. Ritchie, T.N. Alliston et al., J. Bone Miner. Res. 33(6), 1066 (2018)
V. Imbeni, R. Nalla, C. Bosi, J. Kinney, R. Ritchie, J. Biomed. Mater. Res. Part A Off. J. Soc. Biomater. Jpn. Soc. Biomater. Aust. Soc. Biomater. Korean Soc. Biomater. 66(1), 1 (2003)
M. Sieverts, Y. Obata, J.L. Rosenberg, W. Woolley, D.Y. Parkinson, H.S. Barnard, D.M. Pelt, C. Acevedo, Commun. Mater. 3(1), 1 (2022)
R.K. Nalla, J.H. Kinney, R.O. Ritchie, Nat. Mater. 2(3), 164 (2003)
M. Bath-Balogh, M.J. Fehrenbach, Illus. Dental Embryol. Histol. Anat. Inst. Resour. Manual 5, 160 (2006)
X. Feng, Curr. Chem. Biol. 3(2), 189 (2009)
J.-Y. Rho, L. Kuhn-Spearing, P. Zioupos, Med. Eng. Phys. 20(2), 92 (1998)
F. Baino, Biomedical, Therapeutic and Clinical Applications of Bioactive Glasses (2018), pp. 443–466
Y. Wang, T. Azaïs, M. Robin, A. Vallée, C. Catania, P. Legriel, G. Pehau-Arnaudet, F. Babonneau, M.-M. Giraud-Guille, N. Nassif, Nat. Mater. 11(8), 724 (2012)
W. Nijhuis, D. Eastwood, J. Allgrove, I. Hvid, H. Weinans, R. Bank, R. Sakkers, J. Child. Orthop. 13(1), 1 (2019)
Y. Lin, S. Xu, J. Microsc. 241(3), 291 (2011)
B. Yu, A. Pacureanu, C. Olivier, P. Cloetens, F. Peyrin, Sci. Rep. 10(1), 4567 (2020)
V. Sansalone, J. Kaiser, S. Naili, T. Lemaire, Biomech. Model. Mechanobiol. 12(3), 533–553 (2013)
E. Vennat, W. Wang, R. Genthial, B. David, E. Dursun, A. Gourrier, Acta Biomater. 51, 418–432 (2017)
I. Mjör, I. Nordahl, Arch. Oral Biol. 41(5), 401–412 (1996)
J. Kinney, J. Pople, G. Marshall, S. Marshall, Calcif. Tissue Int. 69(1), 31 (2001)
J. Kim, G. Lee, W.S. Chang, S.H. Ki, J.-C. Park, J. Bone Metab. 28(1), 1 (2021)
T. Orvig, Structural and Chemical Organization of Teeth (1967), pp. 45–110
K. Kawasaki, A.V. Buchanan, K.M. Weiss, Cells Tissues Org. 186(1), 7 (2007)
M. Goldberg, A.B. Kulkarni, M. Young, A. Boskey, Front. Biosci. (Elite Ed.) 3, 711 (2011)
S.O. Vital, C. Gaucher, C. Bardet, P. Rowe, A. George, A. Linglart, C. Chaussain, Bone 50(4), 989 (2012)
P. Zioupos, J. Currey, A. Hamer, J. Biomed. Mater. Res. Off. J. Soc. Biomater. Jpn. Soc. Biomater. Aust. Soc. Biomater. 45(2), 108 (1999)
X. Wang, X. Shen, X. Li, C.M. Agrawal, Bone 31(1), 1 (2002)
N.V. Kuznetsova, D.J. McBride Jr., S. Leikin, J. Mol. Biol. 331(1), 191 (2003)
X. Wang, X. Li, R. Bank, Agrawal C. Bone 4, 11 (2002)
S. Li, E. Demirci, V.V. Silberschmidt, J. Mech. Behav. Biomed. Mater. 21, 109 (2013)
A. Mayya, A. Banerjee, R. Rajesh, Sci. Rep. 3(1), 1 (2013)
K.E. Stockhausen, M. Qwamizadeh, E.M. Wölfel, H. Hemmatian, I.A. Fiedler, S. Flenner, E. Longo, M. Amling, I. Greving, R.O. Ritchie et al., ACS Nano 15(1), 455 (2021)
W. Wagermaier, S. Gupta, H.A. Gourrier, M. Burghammer, P. Roschger, P. Fratzl, Biointerphases 1(1), 1 (2006)
H. Ryou, N. Amin, A. Ross, N. Eidelman, D. Wang, E. Romberg, D. Arola, J. Mater. Sci. Mater. Med. 22, 1127 (2011)
Y. Li, S.M. Yu, Collagen: Methods and Protocols (2019), pp. 135–144
A.H. Lin, J.L. Zitnay, Y. Li, S.M. Yu, J.A. Weiss, J. Orthop. Res. 37(2), 431 (2019)
E. Makareeva, E.L. Mertz, N.V. Kuznetsova, M.B. Sutter, A.M. DeRidder, W.A. Cabral, A.M. Barnes, D.J. McBride, J.C. Marini, S. Leikin, J. Biol. Chem. 283(8), 4787 (2008)
R.F. Pereira, E.L. Hume, K.W. Halford, D.J. Prockop, J. Bone Miner. Res. 10(12), 1837 (1995)
V. Mann, E.E. Hobson, B. Li, T.L. Stewart, S.F. Grant, S.P. Robins, R.M. Aspden, S.H. Ralston et al., J. Clin. Investig. 107(7), 899 (2001)
M. Bernad, M. Martinez, M. Escalona, M. Gonzalez, C. Gonzalez, M. Garces, M. Del Campo, E.M. Mola, R. Madero, L. Carreno, Bone 30(1), 223 (2002)
A. Mieczkowska, S.A. Mansur, N. Irwin, P.R. Flatt, D. Chappard, G. Mabilleau, Bone 76, 31 (2015)
S. Viguet-Carrin, P. Garnero, P. Delmas, Osteoporos. Int. 17(3), 319 (2006)
R. Martin, J. Ishida, J. Biomech. 22(5), 419 (1989)
P.V. Taufalele, J.A. VanderBurgh, A. Muñoz, M.R. Zanotelli, C.A. Reinhart-King, PLoS ONE 14(5), 0216537 (2019)
C.A. Miles, A.J. Bailey, In: Proceedings of the Indian Academy of Sciences-Chemical Sciences, vol. 111 (Springer, 1999). pp. 71–80
R. Fraser, T. MacRae, E. Suzuki, J. Mol. Biol. 129(3), 463 (1979)
S.P. Robins, A.J. Bailey, Biochem. J. 149(2), 381 (1975)
L. Bozec, M. Odlyha, Biophys. J. 101(1), 228 (2011)
K. Tai, PhD thesis, Massachusetts Institute of Technology (2007)
M.F. Paige, J.K. Rainey, M.C. Goh, Biophys. J. 74(6), 3211 (1998)
A. Forlino, W.A. Cabral, A.M. Barnes, J.C. Marini, Nat. Rev. Endocrinol. 7(9), 540 (2011)
A. Stylianou, Materials 15(4), 1608 (2022)
B. Zeller-Plumhoff, C. Malich, D. Krüger, G. Campbell, B. Wiese, S. Galli, A. Wennerberg, R. Willumeit-Römer, D.F. Wieland, Acta Biomater. 101, 637 (2020)
U. Amornkitbamrung, Y. In, Z. Wang, J. Song, S.H. Oh, M.-H. Hong, H. Shin, ACS Omega 7(6), 4821 (2022)
Y. In, U. Amornkitbamrung, M.-H. Hong, H. Shin, ACS Omega 5(42), 27204 (2020)
R.K. Nalla, J.J. Kruzic, R.O. Ritchie, Bone 34(5), 790 (2004)
K.J. Koester, J. Ager, R. Ritchie, Nat. Mater. 7(8), 672 (2008)
Y. Liu, A. Li, X. Lin, In: IOP Conference Series: Earth and Environmental Science, vol. 512, (IOP Publishing, 2020), p. 012148
N. Iwamoto, N.D. Ruse, J. Biomed. Mater. Res. Part A Off. J. Soc. Biomater. Jpn. Soc. Biomater. Aust. Soc. Biomater. Korean Soc. Biomater. 66(3), 507 (2003)
S.T. Rasmussen, R.E. Patchin, D.B. Scott, A.H. Heuer, J. Dent. Res. 55(1), 154 (1976)
S. Rasmussen, R. Patchin, J. Dent. Res. 63(12), 1362 (1984)
E. Donnelly, D.X. Chen, A.L. Boskey, S.P. Baker, M.C. van der Meulen, Calcif. Tissue Int. 87(5), 450 (2010)
E.F. Morgan, M.L. Bouxsein, Principles Bone Biol. 1, 29 (2002)
A.H. Burstein, J. Zika, K. Heiple, L. Klein, JBJS 57(7), 956–961 (1975)
E. Lucchinetti, Bone Mechanics Handbook 2 (2001)
E.A. Zimmermann, E. Schaible, H. Bale, H.D. Barth, S.Y. Tang, P. Reichert, B. Busse, T. Alliston, J.W. Ager III., R.O. Ritchie, Proc. Natl. Acad. Sci. 108(35), 14416 (2011)
A. Bigham-Sadegh, A. Oryan, Int. Wound J. 12(3), 238 (2015)
X. Wang, R.A. Bank, J.M. TeKoppele, C.M. Agrawal, J. Orthop. Res. 19(6), 1021 (2001)
K. Beck, V.C. Chan, N. Shenoy, A. Kirkpatrick, J.A. Ramshaw, B. Brodsky, Proc. Natl. Acad. Sci. 97(8), 4273 (2000)
S.F. Lipson, J.L. Katz, J. Biomech. 17(4), 231 (1984)
A.A. Abdel-Wahab, K. Alam, V.V. Silberschmidt, J. Mech. Behav. Biomed. Mater. 4(5), 807 (2011)
Acknowledgements
This work has been supported as part of France 2030 program ANR-11-IDEX-0003.
Author information
Authors and Affiliations
Contributions
CA and EV designed research; QW, TR and MV performed research; QW, ST analyzed data; CA, EV, QW, ST wrote the manuscript. All authors have given approval for the final version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wu, Q., Touraivane, S., Reiss, T. et al. Multiscale Effects of Collagen Damage in Cortical Bone and Dentin. JOM 75, 2102–2113 (2023). https://doi.org/10.1007/s11837-023-05852-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11837-023-05852-0