Investigating the Mechanical Characteristics of Bone-Metal Implant Interface Using in situ Synchrotron Tomographic Imaging

Abstract

Long-term stability of endosseous implants depends on successful bone formation, ingrowth and adaptation to the implant. Specifically, it will define the mechanical properties of the newly formed bone-implant interface. 3D imaging during mechanical loading tests (in situ loading) can improve the understanding of the local processes leading to bone damage and failure. In this study, titanium screws were implanted into rat tibiae and were allowed to integrate for 4 weeks with or without the addition of the growth factor Bone Morphogenetic Protein and the bisphosphonate Zoledronic Acid. Samples were subjected to in situ pullout using high-resolution synchrotron x-ray tomography at the Tomcat beamline (SLS, PSI, Switzerland) at 30 keV with 25 ms exposure time, resulting in a total acquisition time of 45 s per scan, with a 3.6 μm isotropic voxel size. Using a custom-made loading device positioned inside the beamline, screws were pulled out with 0.05 mm increment, acquiring multiple scans until rupture of the sample. The in situ loading protocol was adapted to ensure short imaging time, which enabled multiple samples to be tested with short loading steps, while keeping the total testing time low and reducing dose deposition. Higher trabecular bone content was quantified in the surrounding of the screw in the treated groups, which correlated with increased mechanical strength and stiffness. Differences in screw implantation, such as contact between threads and cortex as well as minor tilt of the screw were also correlated to the mechanical parameters. In situ loading enabled the investigation of crack propagation during the pullout, highlighting the mechanical behavior of the interface. Three typical crack types were observed: (1) rupture at the interface of trabecular and cortical bone tissues, close to the screw, (2) large crack inside the cortex connected to the implant, and (3) first failure away from the screw with cracks propagating toward the screw-bone interface. Mechanical properties of in vivo integrated bone-metal screws rely on a combination of multiple parameters that are difficult to identify and separate one from the other.

Keywords: X-ray tomography; bone; in situ loading; metallic screw; synchrotron.

Figure 1

(A) Overview of the in situ loading set-up at TOMCAT beamline, SLS, PSI, Switzerland. (B) Custom made loading device used to pull the screw out of the tibia (sample placement is illustrated without surrounding chamber). The blue arrow indicates the pull-out direction.

Figure 2

(A) Screw insertion parameters showing distance (d) between the screw and the tibial plateau as well as tilt (t) measured on a 2D radiograph. (B) Trabecular ROI started 1 mm proximal to the screw edge and ended 1 mm distal to the screw edge (i). ROI included trabecular bone and excluded the cortex as drawn in yellow in original (ii) and segmented (iii), as exemplified in three transversal cuts from the unloaded scan.

Figure 3

Contact between screw threads and cortex (A) and bone volume fraction in ROI defined in Figures 2 (B) for each treatment group presented with box-and-whisker plots showing the range of the data, the quartiles, and the median; ^*represents p < 0.05. In insert are illustrated the cutting planes used in (C,D): transversal (i, full line) and longitudinal (ii, dotted line). (C) Partial cuts of cortical bone (beige) segmentation to visualize the contact with the screw (light red: whole contact, dark red: with threads) for a typical sample from each treatment group. (D) Cuts of raw scans to visualize trabecular bone in the same samples. Data in (C) is presented in 3D as (Supplementary Data Sheets S1–S3 for respectively control, BMP and BMP + Za samples).

Figure 4

Maximum force and stiffness (A,B) presented as box-and-whisker plots showing the range of the data, the quartiles, and the median; ^*represents p < 0.05. Significant (p < 0.05) correlations obtained between stiffness (C,E) and maximum force (D,F) with BV/TV and screw insertion are shown with Spearman correlation coefficient ρ, p-value and R-squared value of linear regression curve.

Figure 5

Typical crack patterns from 2D slice cuts (A) from two steps before rupture (left) to the step at or immediately after rupture (right). Yellow arrows indicate the main cracks. Data in (A) is presented as GIF in Supplementary Data Sheets (S4–S6 for respectively Crack Type 1, Type 2, and Type 3 samples). (B) Force vs. displacement curves during in situ pullout of all samples in each crack group, where the dark blue curves are control samples and the light orange curves are BMP + Za samples. Crack Type 1 showed rupture close to screw mainly inside trabecular bone. Crack Type 2 failed through large cortical cracks. Crack Type 3 indicates that failure started presumably away from the screw and propagated toward the interface.