Characterizing mineral ellipsoids in new bone formation at the interface of Ti6Al4V porous implants

Deering, Joseph; Chen, Jianyu; Mahmoud, Dalia; Tang, Tengteng; Lin, Yujing; Fang, Qiyin; Wohl, Gregory R.; Elbestawi, Mohamed; Grandfield, Kathryn

Affiliations

¹Department of Materials Science and Engineering, McMaster University, Hamilton, ON L8S 4L8, Canada

²Guanghua School of Stomatology, Hospital of Stomatology, Guangdong Provincial Key Laboratory of Stomatology, Sun Yat-sen University, Guangzhou 510055, China

³Department of Mechanical Engineering, McMaster University, Hamilton, ON L8S 4L8, Canada

⁴Production Engineering Department, Faculty of Engineering, Alexandria University, Alexandria 21544, Egypt

⁵Department of Engineering Physics, McMaster University, Hamilton, ON L8S 4L8, Canada

⁶School of Biomedical Engineering, McMaster University, Hamilton, ON L8S 4L8, Canada

⁷Brockhouse Institute for Materials Research, McMaster University, Hamilton, ON L8S 4L8, Canada

Abstract and keywords

The hierarchy of newly formed bone contains elements of disorder within an ordered multiscale structure, spanning from the macroscale to below the nanoscale. With mineralized structures presenting in the shape of ellipsoids in mature and mineralizing tissue, this work characterizes the heterogeneity in the mineral ellipsoid packing at the interface of porous titanium implants. Using scanning transmission electron microscopy and plasma-focused ion beam–scanning electron microscopy, mineral ellipsoids are characterized at the implant interface in both 2D and 3D. Heterogeneous in their size and shape within the newly formed bone tissue, ellipsoids are observed with alternating orientations corresponding to unique lamellar packets within 23 µm of the titanium implant interface—although this motif is not universal, and a mineral-dense zone can also appear at the implant interface. Short-order ellipsoid orientation shifts are also present in the 3D probe of the implant interface, where a ≈90° misorientation angle between neighboring packets of mineral ellipsoids (and an intervening organic layer) resolves with increasing distance from the titanium. Combined with local patches of woven-to-lamellar transition, the early heterogeneity and transformation of peri-implant bone structure is a quintessential step in the development of a functional connection between implant and bone.

Keywords: additive manufacturing; bone structure; bone–implant interface; mineral ellipsoid; osseointegration; plasma focused ion beam; porous implant

Links

DOI: 10.1002/admi.202300333

WoS: 001033727900001

History

Received: 2023-06-01

Revised: 2023-07-05

Online: 2023-07-23

Cited Works (16)

Year	Entry
2018	Hasegawa T, Yamamoto T, Hongo H, Qiu Z, Abe M, Kanesaki T, Tanaka K, Endo T, de Freitas PHL, Li M, Amizuka N. Three-dimensional ultrastructure of osteocytes assessed by focused ion beam-scanning electron microscopy (FIB-SEM). Histochem Cell Biol. April 2018;149(4):423-432.
2018	Shah FA, Thomsen P, Palmquist A. A review of the impact of implant biomaterials on osteocytes. J Dent Res. August 2018;97(9):977-986.
1993	Landis WJ, Song MJ, Leith A, McEwen L, McEwen BF. Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high-voltage electron microscopic tomography and graphic image reconstruction. J Struct Biol. January 1993;110(1):39-54.
2018	Grandfield K, Vuong V, Schwarcz HP. Ultrastructure of bone: hierarchical features from nanometer to micrometer scale revealed in focused ion beam sections in the TEM. Calcif Tiss Int. December 2018;103(6):606-616.
2020	Buss DJ, Reznikov N, McKee MD. Crossfibrillar mineral tessellation in normal and Hyp mouse bone as revealed by 3D FIB-SEM microscopy. J Struct Biol. November 1, 2020;212(2):107603.
2014	Reznikov N, Shahar R, Weiner S. Three-dimensional structure of human lamellar bone: the presence of two different materials and new insights into the hierarchical organization. Bone. February 2014;59:93-104.
2020	Yu B, Pacureanu A, Olivier C, Cloetens P, Peyrin F. Assessment of the human bone lacuno-canalicular network at the nanoscale and impact of spatial resolution. Sci Rep. 2020;10:4567.
2017	Wang X, Shah FA, Palmquist A, Grandfield K. 3D characterization of human nano-osseointegration by on-axis electron tomography without the missing wedge. ACS Biomater Sci Eng. 2017;3(1):49-55.
2021	Micheletti C, Gomes-Ferreira PHS, Casagrande T, Lisboa-Filho PN, Okamoto R, Grandfield K. From tissue retrieval to electron tomography: nanoscale characterization of the interface between bone and bioactive glass. J R Soc Interface. September 2021;18(182):20210181.
2022	Micheletti C, Hurley A, Gourrier A, Palmquist A, Tang T, Shah FA, Grandfield K. Bone mineral organization at the mesoscale: a review of mineral ellipsoids in bone and at bone interfaces. Acta Biomater. April 1, 2022;142:1-13.
2020	Binkley DM, Deering J, Yuan H, Gourrier A, Grandfield K. Ellipsoidal mesoscale mineralization pattern in human cortical bone revealed in 3D by plasma focused ion beam serial sectioning. J Struct Biol. November 1, 2020;212(2):107615.
1988	Giraud-Guille MM. Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tiss Int. May 1988;42(3):167-180.
1968	Ascenzi A, Bonucci E. The compressive properties of single osteons. Anat Rec. July 1968;161(3):377-392.
2014	Reznikov N, Shahar R, Weiner S. Bone hierarchical structure in three dimensions. Acta Biomater. September 2014;10(8):3815-3826.
2018	Reznikov N, Bilton M, Lari L, Stevens MM, Kröger R. Fractal-like hierarchical organization of bone begins at the nanoscale. Science. May 4, 2018;360(6388):eaao2189.
2015	Buenzli PR, Sims NA. Quantifying the osteocyte network in the human skeleton. Bone. June 2015;75:144-150.

Cited By (2)

Year	Entry
2024	Tang T, Casagrande T, Mohammadpour P, Landis W, Lievers B, Grandfield K. Characterization of human trabecular bone across multiple length scales using a correlative approach combining X-ray tomography with LaserFIB and plasma FIB-SEM. Sci Rep. September 16, 2024;14:21604.
2023	Micheletti C. Multimodal and Multiscale Characterization of Bone and Bone Interfaces in Health and Disease [PhD thesis]. University of Gothenburg; 2023.