Biomechanical adaptation of the bone-periodontal ligament (PDL)-tooth fibrous joint as a consequence of disease - PubMed (original) (raw)

Biomechanical adaptation of the bone-periodontal ligament (PDL)-tooth fibrous joint as a consequence of disease

Jeremy D Lin et al. J Biomech. 2014.

Abstract

In this study, an in vivo ligature-induced periodontitis rat model was used to investigate temporal changes to the solid and fluid phases of the joint by correlating shifts in joint biomechanics to adaptive changes in soft and hard tissue morphology and functional space. After 6 and 12 weeks of ligation, coronal regions showed a significant decrease in alveolar crest height, increased expression of TNF-α, and degradation of attachment fibers as indicated by decreased collagen birefringence. Cyclical compression to peak loads of 5-15N at speeds of 0.2-2.0mm/min followed by load relaxation tests showed decreased stiffness and reactionary load rate values, load relaxation, and load recoverability, of ligated joints. Shifts in joint stiffness and reactionary load rate increased with time while shifts in joint relaxation and recoverability decreased between control and ligated groups, complementing measurements of increased tooth displacement as evaluated through digital image correlation. Shifts in functional space between control and ligated joints were significantly increased at the interradicular (Δ10-25μm) and distal coronal (Δ20-45μm) regions. Histology revealed time-dependent increases in nuclei elongation within PDL cells and collagen fiber alignment, uncrimping, and directionality, in 12-week ligated joints compared to random orientation in 6-week ligated joints and to controls. We propose that altered strains from tooth hypermobility could cause varying degrees of solid-to-fluid compaction, alter dampening characteristics of the joint, and potentiate increased adaptation at the risk of joint failure.

Keywords: Biomechanical adaptation; Biomechanics; Bone–PDL–tooth fibrous joint; Periodontal ligament; Periodontitis; Stiffness.

Published by Elsevier Ltd.

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Conflict of interest statement

Conflict of Interest Statement: We acknowledge that all authors do not have any conflict of interest and were fully involved in the study and preparation of the manuscript.

Figures

Figure 1. Biomechanical response to simulated cyclical physiological loads

Load rate versus displacement rate plots compare the reactionary load rate response of fibrous joints after 6 weeks (A; control – black, ligated – green) and 12 weeks (B; control – blue, ligated – red) of ligation. Linear trend lines are fitted through each group of data points from each reactionary peak load using the least squares method. Stiffness versus displacement plots compare the stiffness response of fibrous joints after 6 weeks (C; control – black, ligated – green) and 12 weeks (D; control – blue, ligated – red) of ligation. Trend lines are plotted through each group of data point from each displacement rate. Color-coded boxes highlight the differences in displacement ranges between control and ligated groups. Column plots were used to illustrate the differences in slopes between control and ligated groups (control value subtracted from ligated value) at each time point (6-week – black, 12-week – gray) as measured from load rate-displacement rate (E) and stiffness-displacement (F) graphs. Disp. – displacement.

Figure 2. Load relaxation response under constant displacement

(A) Representative load versus time and corresponding displacement versus time plots illustrate the typical loading, hold, and unloading phases of each loading cycle. The hold phase used for load relaxation analysis, during which the displacement is held constant, is highlighted in orange. Load relaxation profiles compare control and ligated fibrous joints that underwent loading at 0.2mm/min (B) and 2.0mm/min (C) at the 6-week time point and 0.2mm/min (D) and 2.0mm/min (E) at the 12-week time point. Time values are plotted in logarithmic scale of base 10. Curves are offset for effective comparisons between control and ligated groups at each reactionary peak load. As such, the top row of graphs represents the hold phase of cycles loaded to a reactionary peak load of 15N, the second row represents those loaded to 10N, and the final row represents those loaded to 5N. 6-week control – black; 6-week ligated – green; 12-week control – blue; 12-week ligated – red.

Figure 3. Load recovery response during unloading

(A) Representative load versus time and corresponding displacement versus time plots illustrate the typical loading, hold, and unloading phases of each loading cycle. The unloading phase used for load recovery analysis is highlighted in orange. Load recovery profiles compare control and ligated fibrous joints that underwent loading at 0.2mm/min (B) and 2.0mm/min (C) at the 6-week time point and 0.2mm/min (D) and 2.0mm/min (E) at the 12-week time point. Curves were offset to for effective comparisons between control and ligated groups at each reactionary peak load. For each individual graph, the set of curves decreasing from 0N represents the unloading phase of cycles loaded to a reactionary peak load of 5N, the set of curves decreasing from −5N represents those loaded to 10N, and the final set of curves decreasing from −10N represents those loaded to 15N. Equivalent column plots compare initial unloading load rates at 0.2mm/min (F) and 2.0mm/min (G) of unloading between control (solid) and ligated (dotted) fibrous joints after 6 weeks (black) and 12 weeks (gray) of ligation. (B-E) 6-week control – black; 6-week ligated – green; 12-week control – blue; 12-week ligated – red.

Figure 4. Calculated tooth displacement within the alveolar bone socket using digital image correlation (DIC)

Comparisons in tooth displacement relative to the bone within control (A,B) and ligated (C,D) joints. Color-coded regions indicate areas analyzed for changes in horizontal (X-axis, A, C) and vertical (Y-axis, B, D) displacement fields. Each color represents a different displacement range. Please note the axis and displacement range changes for displacement vectors between control and ligated joints. Circular arrows are representative (not to scale) indicators of the direction and magnitude of tooth movement based on calculated DIC values.

Figure 5. Correlation between morphometrics and osteoclastic activity as analyzed through PDL-width and TRAP staining

(A) The column graph shows differences in average PDL-space measurements between control and ligated fibrous joints (control values subtracted from ligated values) at interradicular (red), mesial coronal (grey), mesial apical (green), distal coronal (orange), and distal apical (blue) regions. Both 6-week (solid) and 12-week (hashed) time points are plotted. Positive values indicate increased PDL-space in ligated joints compared to controls while negative values indicate decreased PDL-space in ligated joints compared to controls. α, β, γ, δ Significant difference between ligated and control within each region (Student's t-test, P<0.05). (B) Light micrograph images taken at 10× magnification compare localization and intensity of TRAP(+) staining within osteoclasts, reversal lines, and the extracellular matrix of control (i-iv, ix, xi-xiv, xix) and ligated (v-viii, x, xv-viii, xx) joints after 6 weeks (i-x) and 12 weeks (xi-xx) of ligation. At 6 weeks, differences are annotated in distal (light blue arrows) and mesial furcation (brown arrows). At 12 weeks, differences are noted in mesial (yellow arrows), mesial furcation (blue arrows), distal furcation (green arrows), and distal regions (black arrows) are compared. Advancement of secondary cementum is also highlighted (green hashed lines). Please note that tissues within each image were oriented similarly based on corresponding regions of mesial coronal, mesial apical, distal coronal, distal apical, and interradicular. T – tooth; B – bone; PDL – periodontal ligament; SC – secondary cementum.

Figure 6. Histological observations of collagen fiber orientation, shape, and organization

(A) Representative H&E-stained sections at 10× magnification show interproximal gingiva adjacent to the second molar of 6-week control (i), 6-week ligated (ii), 12-week control (iii), and 12-week ligated (iv) rats. Representative micrographs of corresponding H&E-stained (10× magnification; B.i-iv, C.i-iv) and PSR-stained (4× magnification; B.v-viii, C.v-viii) sections compare differences in the apical mesial and distal regions of control and ligated fibrous joints at 6-week (B) and 12-week (C) time points. (B.i-iv, C.i-iv) Differences in morphology of nuclei (along hashed arrows) and advancement of the mineralization front (green asterisks) are highlighted. (B.v-viii, C.v-viii) Images of PSR-stained sections were taken using polarized light. Plots illustrate directionality of birefringent collagen fibers within mesial apical (B.ix, C.ix), distal coronal (B.x, C.x), and distal apical regions (B.xi, C.xi). Color coding within plots correspond to colored boxes within micrographs. T – tooth; IE – interdental epithelium; TF – transseptal fibers; Lig – ligature; B – bone; PDL – periodontal ligament; SC – secondary cementum.

Figure 6. Histological observations of collagen fiber orientation, shape, and organization

Figure 7. Suggested model summarizing the findings in a temporal fashion

(A) These observations are based on the hallmarks of periodontitis, joint biomechanics, and morphological features of the soft tissue and the overall joint. Polygonal shapes illustrate deviation of the diseased joint from the control joint based on magnitude. The negligible differences at the beginning of the timeline represent no differences in baseline measurements between the two groups at the start of ligation. Arrows represent the increase and/or decrease in deviation. (B) Illustrations showing the suggested differences in permeability that correlate to the findings at both the early stages (4-15 days) (Lee and Lin et al., 2013) and later stages (6-12 weeks) of the study. Permeability to fluid flux is expected to increase during the initial degradative phase of the disease, during which the host response to inflammation causes degeneration of transseptal fibers and a decrease in crestal bone height. Strain-induced adaptation due to the increased mobility of the tooth is observed within the apical regions of the PDL at later stages of periodontitis, leading to increased fibrous tissue formation and a decrease in proteoglycan content. Permeability of the tissue is decreased leading to a decrease in load relaxation and load recovery characteristics in the diseased fibrous joint at a later stage. As such, the cause of decreased stiffness and load rate is attributed to a loss in PDL attachment and degradation of the coronal aspects of the joint, while the decrease in load relaxation (at higher loads) and recoverability (at lower loads) can be attributed to adaptation of the joint. Please note that the observed biomechanically-induced adaptations outlined in this model are reserved to the soft tissue elements of the fibrous joint.

Figure 7. Suggested model summarizing the findings in a temporal fashion

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Biomechanical adaptation of the bone-periodontal ligament (PDL)-tooth fibrous joint as a consequence of disease - PubMed (original) (raw)