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Strain-guided mineralization in the bone – PDL – cementum complex of a rat periodontium

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ABSTRACT

Objective: The objective of this study was to investigate the effect of mechanical strain by mapping physicochemical properties at periodontal ligament (PDL)–bone and PDL–cementum attachment sites and within the tissues per se.

Design: Accentuated mechanical strain was induced by applying a unidirectional force of 0.06 N for 14 days on molars in a rat model. The associated changes in functional space between the tooth and bone, mineral forming and resorbing events at the PDL–bone and PDL–cementum attachment sites were identified by using micro-X-ray computed tomography (micro-XCT), atomic force microscopy (AFM), dynamic histomorphometry, Raman microspectroscopy, and AFM-based nanoindentation technique. Results from these analytical techniques were correlated with histochemical strains specific to low and high molecular weight GAGs, including biglycan, and osteoclast distribution through tartrate resistant acid phosphatase (TRAP) staining.

Results: Unique chemical and mechanical qualities including heterogeneous bony fingers with hygroscopic Sharpey's fibers contributing to a higher organic (amide III — 1240 cm− 1) to inorganic (phosphate — 960 cm− 1) ratio, with lower average elastic modulus of 8 GPa versus 12 GPa in unadapted regions were identified. Furthermore, an increased presence of elemental Zn in cement lines and mineralizing fronts of PDL–bone was observed. Adapted regions containing bony fingers exhibited woven bone-like architecture and these regions rich in biglycan (BGN) and bone sialoprotein (BSP) also contained high-molecular weight polysaccharides predominantly at the site of polarized bone growth.

Conclusions: From a fundamental science perspective the shift in local properties due to strain amplification at the soft–hard tissue attachment sites is governed by semiautonomous cellular events at the PDL–bone and PDL–cementum sites. Over time, these strain-mediated events can alter the physicochemical properties of tissues per se, and consequently the overall biomechanics of the bone–PDL–tooth complex. From a clinical perspective, the shifts in magnitude and duration of forces on the periodontal ligament can prompt a shift in physiologic mineral apposition in cementum and alveolar bone albeit of an adapted quality owing to the rapid mechanical translation of the tooth.

No MeSH data available.


Related in: MedlinePlus

Fluorochrome images of experimental (a, b) groups reveal irregular patterns of mineralization. Control specimens displayed regular banding patterns which indicated a progressing biomineralization front. Experimental specimens indicate much less organized mineralization and nodules or finger-like protrusions of biomineralization in regions experiencing tension, for example the boxed region, compared to unstrained regions marked by *. Upon closer inspection of D, the strained region shows increased mineralization consistently surrounding blood vessel or endosteal spaces as marked by arrows. The vessels appear to be elongated along the direction of strain, and such a mechanical cue may be contributing to the enhanced mineral formation in their vicinity. Gradients in microprobe XRF elemental mapping are illustrated and are correlated with structural features as indicated by light microscopy technique. A bicolor elemental map for calcium and zinc signals shown in (d) and a corresponding light microscope image in (c). Gradients in (d) show calcium and zinc in existing bone (orange to dark orange), zinc only in areas of new bone growth within PDL (green), and new bone-finger regions high in zinc yet low in calcium (yellow) which correspond to cement lines (also observed in controls) and active sites of remodeling surrounding bone finger protrusions. AB: alveolar bone, NB: new bone, T: tooth, PDL: periodontal ligament.
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f0020: Fluorochrome images of experimental (a, b) groups reveal irregular patterns of mineralization. Control specimens displayed regular banding patterns which indicated a progressing biomineralization front. Experimental specimens indicate much less organized mineralization and nodules or finger-like protrusions of biomineralization in regions experiencing tension, for example the boxed region, compared to unstrained regions marked by *. Upon closer inspection of D, the strained region shows increased mineralization consistently surrounding blood vessel or endosteal spaces as marked by arrows. The vessels appear to be elongated along the direction of strain, and such a mechanical cue may be contributing to the enhanced mineral formation in their vicinity. Gradients in microprobe XRF elemental mapping are illustrated and are correlated with structural features as indicated by light microscopy technique. A bicolor elemental map for calcium and zinc signals shown in (d) and a corresponding light microscope image in (c). Gradients in (d) show calcium and zinc in existing bone (orange to dark orange), zinc only in areas of new bone growth within PDL (green), and new bone-finger regions high in zinc yet low in calcium (yellow) which correspond to cement lines (also observed in controls) and active sites of remodeling surrounding bone finger protrusions. AB: alveolar bone, NB: new bone, T: tooth, PDL: periodontal ligament.

Mentions: Experimental specimens indicated an irregular mineralization pattern with finger-like protrusions on the distal side, and accompanying banding indicating enhanced mineralization of the finger-like regions (Fig. 4a and b). Fig. 4a highlights the increased rate of biomineralization in strained regions (boxed region) compared to less-strained regions (stars, Fig. 4a).


Strain-guided mineralization in the bone – PDL – cementum complex of a rat periodontium
Fluorochrome images of experimental (a, b) groups reveal irregular patterns of mineralization. Control specimens displayed regular banding patterns which indicated a progressing biomineralization front. Experimental specimens indicate much less organized mineralization and nodules or finger-like protrusions of biomineralization in regions experiencing tension, for example the boxed region, compared to unstrained regions marked by *. Upon closer inspection of D, the strained region shows increased mineralization consistently surrounding blood vessel or endosteal spaces as marked by arrows. The vessels appear to be elongated along the direction of strain, and such a mechanical cue may be contributing to the enhanced mineral formation in their vicinity. Gradients in microprobe XRF elemental mapping are illustrated and are correlated with structural features as indicated by light microscopy technique. A bicolor elemental map for calcium and zinc signals shown in (d) and a corresponding light microscope image in (c). Gradients in (d) show calcium and zinc in existing bone (orange to dark orange), zinc only in areas of new bone growth within PDL (green), and new bone-finger regions high in zinc yet low in calcium (yellow) which correspond to cement lines (also observed in controls) and active sites of remodeling surrounding bone finger protrusions. AB: alveolar bone, NB: new bone, T: tooth, PDL: periodontal ligament.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4663464&req=5

f0020: Fluorochrome images of experimental (a, b) groups reveal irregular patterns of mineralization. Control specimens displayed regular banding patterns which indicated a progressing biomineralization front. Experimental specimens indicate much less organized mineralization and nodules or finger-like protrusions of biomineralization in regions experiencing tension, for example the boxed region, compared to unstrained regions marked by *. Upon closer inspection of D, the strained region shows increased mineralization consistently surrounding blood vessel or endosteal spaces as marked by arrows. The vessels appear to be elongated along the direction of strain, and such a mechanical cue may be contributing to the enhanced mineral formation in their vicinity. Gradients in microprobe XRF elemental mapping are illustrated and are correlated with structural features as indicated by light microscopy technique. A bicolor elemental map for calcium and zinc signals shown in (d) and a corresponding light microscope image in (c). Gradients in (d) show calcium and zinc in existing bone (orange to dark orange), zinc only in areas of new bone growth within PDL (green), and new bone-finger regions high in zinc yet low in calcium (yellow) which correspond to cement lines (also observed in controls) and active sites of remodeling surrounding bone finger protrusions. AB: alveolar bone, NB: new bone, T: tooth, PDL: periodontal ligament.
Mentions: Experimental specimens indicated an irregular mineralization pattern with finger-like protrusions on the distal side, and accompanying banding indicating enhanced mineralization of the finger-like regions (Fig. 4a and b). Fig. 4a highlights the increased rate of biomineralization in strained regions (boxed region) compared to less-strained regions (stars, Fig. 4a).

View Article: PubMed Central - PubMed

ABSTRACT

Objective: The objective of this study was to investigate the effect of mechanical strain by mapping physicochemical properties at periodontal ligament (PDL)–bone and PDL–cementum attachment sites and within the tissues per se.

Design: Accentuated mechanical strain was induced by applying a unidirectional force of 0.06 N for 14 days on molars in a rat model. The associated changes in functional space between the tooth and bone, mineral forming and resorbing events at the PDL–bone and PDL–cementum attachment sites were identified by using micro-X-ray computed tomography (micro-XCT), atomic force microscopy (AFM), dynamic histomorphometry, Raman microspectroscopy, and AFM-based nanoindentation technique. Results from these analytical techniques were correlated with histochemical strains specific to low and high molecular weight GAGs, including biglycan, and osteoclast distribution through tartrate resistant acid phosphatase (TRAP) staining.

Results: Unique chemical and mechanical qualities including heterogeneous bony fingers with hygroscopic Sharpey's fibers contributing to a higher organic (amide III — 1240 cm− 1) to inorganic (phosphate — 960 cm− 1) ratio, with lower average elastic modulus of 8 GPa versus 12 GPa in unadapted regions were identified. Furthermore, an increased presence of elemental Zn in cement lines and mineralizing fronts of PDL–bone was observed. Adapted regions containing bony fingers exhibited woven bone-like architecture and these regions rich in biglycan (BGN) and bone sialoprotein (BSP) also contained high-molecular weight polysaccharides predominantly at the site of polarized bone growth.

Conclusions: From a fundamental science perspective the shift in local properties due to strain amplification at the soft–hard tissue attachment sites is governed by semiautonomous cellular events at the PDL–bone and PDL–cementum sites. Over time, these strain-mediated events can alter the physicochemical properties of tissues per se, and consequently the overall biomechanics of the bone–PDL–tooth complex. From a clinical perspective, the shifts in magnitude and duration of forces on the periodontal ligament can prompt a shift in physiologic mineral apposition in cementum and alveolar bone albeit of an adapted quality owing to the rapid mechanical translation of the tooth.

No MeSH data available.


Related in: MedlinePlus