Determination of the dynamics of healing at the tissue-implant interface by means of microcomputed tomography and functional apparent moduli

Abstract

Purpose: It is currently a challenge to determine the biomechanical properties of the hard tissue-dental implant interface. Recent advances in intraoral imaging and tomographic methods, such as microcomputed tomography (micro-CT), provide three-dimensional details, offering significant potential to evaluate the bone-implant interface, but yield limited information regarding osseointegration because of physical scattering effects emanating from metallic implant surfaces. In the present study, it was hypothesized that functional apparent moduli (FAM), generated from functional incorporation of the peri-implant structure, would eliminate the radiographic artifact-affected layer and serve as a feasible means to evaluate the biomechanical dynamics of tissue-implant integration in vivo.

Materials and methods: Cylindric titanium mini-implants were placed in osteotomies and osteotomies with defects in rodent maxillae. The layers affected by radiographic artifacts were identified, and the pattern of tissue-implant integration was evaluated from histology and micro-CT images over a 21-day observation period. Analyses of structural information, FAM, and the relationship between FAM and interfacial stiffness (IS) were done before and after eliminating artifacts.

Results: Physical artifacts were present within a zone of about 100 to 150 Μm around the implant in both experimental defect situations (osteotomy alone and osteotomy + defect). All correlations were evaluated before and after eliminating the artifact-affected layers, most notably during the maturation period of osseointegration. A strong correlation existed between functional bone apparent modulus and IS within 300 Μm at the osteotomy defects (r > 0.9) and functional composite tissue apparent modulus in the osteotomy defects (r > 0.75).

Conclusion: Micro-CT imaging and FAM were of value in measuring the temporal process of tissue-implant integration in vivo. This approach will be useful to complement imaging technologies for longitudinal monitoring of osseointegration.

Fig 1

Animal surgery. (a) 1-mm-diameter titanium implant in a rat maxilla in the osteotomy-alone (OA) group. (b) In the osteotomy– osseous defect (OS) group, a 0.6 × 1-mm circumferential osseous implant was created around the implant.

Fig 2. Effects of metal scattering on micro-CT imaging

Fig 2a Three-dimensional micro-CT image. A single slice was selected from the central sagittal plane crossing in the osseous defect (grey plane). Figs 2b and 2c Two-dimensional slices of micro-CT imaging (left) before and (right) after implant placement. The area marked by the dashed line refers to the space occupied by the titanium implant; the yellow line indicates the OS defect region; the blue line indicates the OA region. Figs 2d and 2e Distribution of HU values before and after implant placement. (d) In the OS area, a 126-μm blurred zone (gray zones) on the left and a 162-μm zone on the right side of the implant were noted. (e) In the OA area, a 108-μm radiographic artifact (gray zones) was noted on both sides of the implant.

Fig 3

Figs 3a to 3d The FE model for calculating FBAM and FCAM. IM = titanium implant; G = granulation tissue; NB = native bone; MS = maxillary sinus; asterisks refer to area of investigation; purple arrows indicate the direction of simulated load. Fig 3a FBAM for osseous wound repair. Fig 3b FBAM for interfacial osseointegration. Fig 3c FCAM for interfacial osseointegration. Fig 3d FCAM for osseous wound repair.

Fig 4. Bone apposition from the base and lateral walls of osteotomy over time (methylene blue and acid fuchsin; original magnification ×40 in the top row, ×200 in the bottom row)

Figs 4a to 4f Defects in the OA group. At day 10 (left-hand column), a 0- to 50-μm gap (dashed line in the first column) on the interface was filled by new bone. Significant maturation of the interfacial tissue was evident (middle column) on day 14 and (right-hand column) on day 21. Figs 4g to 4i Defects in the OS group. (Left-hand column) A woven trabecular bone structure grew from the border of the defect at day 10. Significant bone maturation and apposition were noted (middle column) on day 14 and (right-hand column) day 21.

Fig 5

Figs 5a to 5d Correlation between functional apparent moduli and interfacial stiffness after eliminating the “artifact layers.” The correlation coefficient between FBAM and IS was examined in the OA group with increasing peri-implant thickness (a) after implant removal and (b) with the implant present, and correlation between peri-implant functional composite tissue apparent modulus (FCAM) and IS was examined in osteotomy plus osseous defect (OS) group with the increasing peri-implant thickness (c) after implant removal and (d) with the implant present. Either the 108-μm or the 162-μm innermost layer was assumed as the “artifact layer” and eliminated for the analyses (ie, analyses started at 126 and 180 μm from the interface, respectively).