Abstract
We studied the lamellar level correlations between the local composition and local mechanical properties in the femur of two inbred strains of mice (A/J and C57BL/6J (B6)), with known differences in the average mineralization and long-bone mechanical properties, to gain insights into how their extracellular matrix is mineralized. The local elastic moduli and indentation yield strengths were determined using spherical nanoindentation stress-strain analysis, while Raman spectroscopy was used to determine the local composition around the indents in a total of 11 samples. Our results show a significant difference in the mineral-to-matrix ratio of the two strains of mice, with the A/J mice showing an overall higher mineral-to-matrix ratio and lower carbonate substitution in the mineral. These differences are prominent in the newer bone and become less significant as the bone matures. Additionally, local mineral-to-matrix ratio was found to be a good indicator of the local mechanical properties.
Similar content being viewed by others
References
Z. Fan and J.Y. Rho, J. Biomed. Mater. Res. Part A 67, 208 (2003).
K. Tai, H.J. Qi, and C. Ortiz, J. Mater. Sci. Mater. Med. 16, 947 (2005).
K.J. Goodwin and N.A. Sharkey, J. Orthop. Res. 20, 600 (2002).
M.D. Morris and G.S. Mandair, Clin. Orthop. Relat. Res.® 469, 2160 (2011). https://doi.org/10.1007/s11999-010-1692-y.
G.S. Mandair and M.D. Morris, BoneKEy Rep. 4, 620 (2015). https://doi.org/10.1038/bonekey.2014.115.
M. Kazanci, P. Roschger, E. Paschalis, K. Klaushofer, and P. Fratzl, J. Struct. Biol. 156, 489 (2006).
I.J.W. Ager, R.O. Ritchie, R.K. Nalla, and K.L. Breeden, J. Biomed. Opt. 10, 034012 (2005).
O. Akkus, F. Adar, and M.B. Schaffler, Bone 34, 443 (2004). https://doi.org/10.1016/j.bone.2003.11.003.
J. Ramasamy and O. Akkus, J. Biomech. 40, 910 (2007).
S. Gamsjaeger, A. Masic, P. Roschger, et al., Bone 47, 392 (2010).
A. Grey, R. Ames, R. Matthews, and I. Reid, Thorax 48, 589 (1993).
A. Boskey and N. Pleshko Camacho, Biomaterials 28, 2465 (2007).
A.L. Boskey, E. Donnelly, E. Boskey, L. Spevak, Y. Ma, W. Zhang, J. Lappe, and R.R. Recker, J. Bone Miner. Res. 31, 1070 (2016).
S. Gourion-Arsiquaud, J.C. Burket, L.M. Havill, et al., J. Bone Miner. Res. 24, 1271 (2009).
J. Burket, S. Gourion-Arsiquaud, L.M. Havill, S.P. Baker, A.L. Boskey, and M.C.H. van der Meulen, J. Biomech. 44, 277 (2011). https://doi.org/10.1016/j.jbiomech.2010.10.018.
Y. Bala, B. Depalle, T. Douillard, et al., J. Mech. Behav. Biomed. Mater. 4, 1473 (2011).
R. Zebaze, A.C. Jones, M.G. Pandy, M.A. Knackstedt, and E. Seeman, Bone 48, 1246 (2011).
B. Achrai and H.D. Wagner, Acta Biomater. 9, 5890 (2013). https://doi.org/10.1016/j.actbio.2012.12.023.
E. Donnelly, A.L. Boskey, S.P. Baker, and M.C.H. van der Meulen, J. Biomed. Mater. Res., Part A 92A, 1048 (2010). https://doi.org/10.1002/jbm.a.32442.
N. Rodriguez-Florez, M.L. Oyen, and S.J. Shefelbine, J. Mech. Behav. Biomed. Mater. 18, 90 (2013). https://doi.org/10.1016/j.jmbbm.2012.11.005.
K. Grover, M. Hu, L. Lin, J. Muir, and Y.-X. Qin, J. Bone Miner. Metab. 37, 1048 (2019).
S. Vennin, A. Desyatova, J.A. Turner, et al., Bone 97, 233 (2017). https://doi.org/10.1016/j.bone.2017.01.031.
J. Schwiedrzik, R. Raghavan, A. Bürki, et al., Nat. Mater. 13, 740 (2014).
O.A. Tertuliano and J.R. Greer, Nat. Mater. 15, 1195 (2016).
A. Groetsch, A. Gourrier, J. Schwiedrzik, et al., Acta Biomater. 89, 313 (2019).
D. Casari, J. Michler, P. Zysset, and J. Schwiedrzik, Acta Biomater. 120, 135 (2021). https://doi.org/10.1016/j.actbio.2020.04.030.
D.M. Ebenstein and L.A. Pruitt, Nano Today 1, 26 (2006). https://doi.org/10.1016/S1748-0132(06)70077-9.
Z. Fan, J.G. Swadener, J.Y. Rho, M.E. Roy, and G.M. Pharr, J. Orthop. Res. 20, 806 (2002). https://doi.org/10.1016/S0736-0266(01)00186-3.
W.G. Beamer, L.R. Donahue, and C.J. Rosen, J. Musculoskelet. Neuronal. Interact. 2, 225 (2002).
C.J. Rosen, W.G. Beamer, and L.R. Donahue, Osteoporos Int. 12, 803 (2001). https://doi.org/10.1007/s001980170030.
K.J. Jepsen, D.E. Pennington, Y.L. Lee, M. Warman, and J. Nadeau, J. Bone Miner. Res. 16, 1854 (2001).
K.J. Jepsen, O.J. Akkus, R.J. Majeska, and J.H. Nadeau, Mamm. Genome 14, 97 (2003).
C. Price, B.C. Herman, T. Lufkin, H.M. Goldman, and K.J. Jepsen, J. Bone Miner. Res. 20, 1983 (2005).
S.R. Kalidindi and S. Pathak, Acta Mater. 56, 3523 (2008).
S. Pathak, J. Shaffer, and S.R. Kalidindi, Scripta Mater. 60, 439 (2009).
B.R. Donohue, A. Ambrus, and S.R. Kalidindi, Acta Mater. 60, 3943 (2012). https://doi.org/10.1016/j.actamat.2012.03.034.
J.-Y. Rho, L. Kuhn-Spearing, and P. Zioupos, Med. Eng. Phys. 20, 92 (1998). https://doi.org/10.1016/S1350-4533(98)00007-1.
J.Y. Rho, P. Zioupos, J.D. Currey, and G.M. Pharr, Bone 25, 295 (1999). https://doi.org/10.1016/S8756-3282(99)00163-5.
S. Hengsberger, J. Enstroem, F. Peyrin, and P. Zysset, J. Biomech. 36, 1503 (2003). https://doi.org/10.1016/S0021-9290(03)00131-3.
M.L. Oyen, J. Biomech. 39, 2699 (2006). https://doi.org/10.1016/j.jbiomech.2005.09.011.
W.C. Oliver and G.M. Pharr, J. Mater. Res. 7, 1564 (1992).
W.C. Oliver and G.M. Pharr, J. Mater. Res. 19, 3 (2004).
S. Pathak, D. Stojakovic, and S.R. Kalidindi, Acta Mater. 57, 3020 (2009).
S. Pathak, J. Michler, K. Wasmer, and S. Kalidindi, J. Mater. Sci. 47, 815 (2012). https://doi.org/10.1007/s10853-011-5859-z.
S.J. Vachhani, C. Trujillo, N. Mara, et al., J. Dyn. Behav. Mater. 2, 511 (2016). https://doi.org/10.1007/s40870-016-0085-z.
S. Pathak, Z.G. Cambaz, S.R. Kalidindi, J.G. Swadener, and Y. Gogotsi, Carbon 47, 1969 (2009).
S. Pathak, S.J. Vachhani, K.J. Jepsen, H.M. Goldman, and S.R. Kalidindi, J. Mech. Behav. Biomed. Mater. 13, 102 (2012).
S. Pathak, J. Gregory Swadener, S.R. Kalidindi, H.-W. Courtland, K.J. Jepsen, and H.M. Goldman, J. Mech. Behav. Biomed. Mater. 4, 34 (2011). https://doi.org/10.1016/j.jmbbm.2010.09.002.
W.G. Beamer, L.R. Donahue, C.J. Rosen, and D.J. Baylink, Bone 18, 397 (1996). https://doi.org/10.1016/8756-3282(96)00047-6.
K.L. Johnson, Indentation Contact Mechanics (Cambridge University Press, Cambridge, 1985).
H. Hertz, Miscellaneous Papers (New York: MacMillan and Co., Ltd., 1896).
A.C. Fischer-Cripps, Vacuum 58, 569 (2000).
S.M. Basu, A. Moseson, and M.W. Barsoum, J. Mater. Res. 21, 2628 (2006). https://doi.org/10.1557/jmr.2006.0324.
S. Pathak, D. Stojakovic, R. Doherty, and S.R. Kalidindi, J. Mater. Res. 24, 1142 (2009).
J.G. Swadener, J.Y. Rho, and G.M. Pharr, J. Biomed. Mater. Res. 57, 108 (2001). https://doi.org/10.1002/1097-4636(200110)57:1<108::AID-JBM1148>3.0.CO;2-6.
A. Carden and M.D. Morris, J. Biomed. Opt. 5, 259 (2000).
J.A. Timlin, A. Carden, and M.D. Morris, Appl. Spectrosc. 53, 1429 (1999). https://doi.org/10.1366/0003702991945786.
Y.N. Yeni, J. Yerramshetty, O. Akkus, C. Pechey, and C.M. Les, Calcif. Tissue Int. 78, 363 (2006). https://doi.org/10.1007/s00223-005-0301-7.
A.L. Boskey, N. Pleshko, S.B. Doty, and R. Mendelsohn, Cells Mater. 2, 209 (1992).
R.G. Miller, Beyond ANOVA, Basics of Applied Statistics (Wiley, New York, 1986).
G. Schwarz, Ann. Stat. 6, 461 (1978).
A.A. Neath and J.E. Cavanaugh, Wiley Interdiscip. Rev. Comput. Stat. 4, 199 (2012).
H.-W. Courtland, P. Nasser, A. Goldstone, L. Spevak, A. Boskey, and K. Jepsen, Calcif. Tissue Int. 83, 342 (2008). https://doi.org/10.1007/s00223-008-9176-8.
H.W. Courtland, M. Spevak, A.L. Boskey, and K.J. Jepsen, Cells Tissues Organs 189, 237 (2009).
C. Huesa, M.C. Yadav, M.A. Finnilä, et al., Bone 48, 1066 (2011).
Acknowledgements
SK and SJV acknowledge funding from ARO Grant W911NF-10-1-0409. SK acknowledges support from ONR award N00014-18-1-2879. SP acknowledges support from NSF BMMB award 1937149, and SJV acknowledges start-up support from Iowa State University during the writing of this article. The authors acknowledge Dr. Haviva Goldman and Dr. Karl Jepsen for providing the specimens used in this study, access to their laboratories for sample preparation as well as the very valuable discussions that helped shape this article. The authors also thank Dr. Phil Nasser and Dr. Hayden-William Courtland (both at Mount Sinai School of Medicine, New York, NY) for assistance with sample preparation as well as Dr. Zhorro Nikolov and Ms. Melanie Patel (Drexel University) for help with Raman measurements. The MTS XP nanoindentation system and the Renishaw 1000 Raman microspectrometer used in this study are maintained and operated by the Centralized Research Facilities in the College of Engineering at Drexel University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vachhani, S.J., Kalidindi, S.R., Burr, T. et al. Lamellar Level Correlations Between Mechanical Behavior and Composition in Mouse Bone. JOM 73, 3034–3045 (2021). https://doi.org/10.1007/s11837-021-04808-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11837-021-04808-6