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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

Immunohistochemistry for bone sialoprotein (BSP) of control and experimental groups. BSP was evenly distributed in primary and secondary cementum as well as alveolar bone in control group (a1). Similar morphological appearance was noticed in experimental groups. However, there are some distinct features to be noticed. Some light-brown stains appear to be associated with bone protrusions (marked with dotted lines in b2, b3) whereas the parent bone shows a strong immunostaining with a mottled appearance. Both control and experimental groups show that BSP is absent in PDL region. This is in accordance with immunolocalization results reported by McKee and Nanci [Ref Cooper et al., 2006]. From polarized microscopic images, the birefringence is more prominent in the cementum–PDL interface and alveolar bone, suggesting the presence of many well aligned collagen fibers. Some birefringence is also noticed in the newly formed bone region for experimental group, indicating strain-mediated modeling process of the bone when subject to strain. These observations suggest strain prompt new bone formation from alveolar bone region at the PDL–bone interface. Enclosed boxes in panels a1 and b1 represent regions, which are tension dominating and shown at higher magnification in panels a2 and b2. Panels a3 and b3 are correspondent to a2 and b2 respectively, when analyzer and polarizer are applied. AB: alveolar bone, PDL: periodontal ligament, C: cementum, NB: new bone, V: blood vessel.
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f0015: Immunohistochemistry for bone sialoprotein (BSP) of control and experimental groups. BSP was evenly distributed in primary and secondary cementum as well as alveolar bone in control group (a1). Similar morphological appearance was noticed in experimental groups. However, there are some distinct features to be noticed. Some light-brown stains appear to be associated with bone protrusions (marked with dotted lines in b2, b3) whereas the parent bone shows a strong immunostaining with a mottled appearance. Both control and experimental groups show that BSP is absent in PDL region. This is in accordance with immunolocalization results reported by McKee and Nanci [Ref Cooper et al., 2006]. From polarized microscopic images, the birefringence is more prominent in the cementum–PDL interface and alveolar bone, suggesting the presence of many well aligned collagen fibers. Some birefringence is also noticed in the newly formed bone region for experimental group, indicating strain-mediated modeling process of the bone when subject to strain. These observations suggest strain prompt new bone formation from alveolar bone region at the PDL–bone interface. Enclosed boxes in panels a1 and b1 represent regions, which are tension dominating and shown at higher magnification in panels a2 and b2. Panels a3 and b3 are correspondent to a2 and b2 respectively, when analyzer and polarizer are applied. AB: alveolar bone, PDL: periodontal ligament, C: cementum, NB: new bone, V: blood vessel.

Mentions: The distribution of BSP was mainly associated with mineralized regions of the tissue such as cementum and alveolar bone as well as newly formed bony protrusions (Fig. 3). BSP was absent in the PDL. The light brown color in the new bone (NB, Fig. 3b2) indicated a lower content of BSP, suggesting an early stage of BSP deposition among other matrix proteins (Fig. 3e). A strong immunostaining was observed in the cementum and alveolar bone, as indicated by the darker brown, suggesting that these mineralized regions could be mature in terms of matrix protein deposition (Fig. 3). Birefringence using polarized light indicated well-aligned collagen fibers at specific regions such as the PDL–cementum and PDL–bone interfaces (Fig. 3a3 and b3). The birefringence in the new bone region is sparse, suggesting that the collagen fibers do not have the same extent of organization (Fig. 3b3). This is consistent with the results obtained from PSR staining (Fig. 2g and h).


Strain-guided mineralization in the bone – PDL – cementum complex of a rat periodontium
Immunohistochemistry for bone sialoprotein (BSP) of control and experimental groups. BSP was evenly distributed in primary and secondary cementum as well as alveolar bone in control group (a1). Similar morphological appearance was noticed in experimental groups. However, there are some distinct features to be noticed. Some light-brown stains appear to be associated with bone protrusions (marked with dotted lines in b2, b3) whereas the parent bone shows a strong immunostaining with a mottled appearance. Both control and experimental groups show that BSP is absent in PDL region. This is in accordance with immunolocalization results reported by McKee and Nanci [Ref Cooper et al., 2006]. From polarized microscopic images, the birefringence is more prominent in the cementum–PDL interface and alveolar bone, suggesting the presence of many well aligned collagen fibers. Some birefringence is also noticed in the newly formed bone region for experimental group, indicating strain-mediated modeling process of the bone when subject to strain. These observations suggest strain prompt new bone formation from alveolar bone region at the PDL–bone interface. Enclosed boxes in panels a1 and b1 represent regions, which are tension dominating and shown at higher magnification in panels a2 and b2. Panels a3 and b3 are correspondent to a2 and b2 respectively, when analyzer and polarizer are applied. AB: alveolar bone, PDL: periodontal ligament, C: cementum, NB: new bone, V: blood vessel.
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Related In: Results  -  Collection

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f0015: Immunohistochemistry for bone sialoprotein (BSP) of control and experimental groups. BSP was evenly distributed in primary and secondary cementum as well as alveolar bone in control group (a1). Similar morphological appearance was noticed in experimental groups. However, there are some distinct features to be noticed. Some light-brown stains appear to be associated with bone protrusions (marked with dotted lines in b2, b3) whereas the parent bone shows a strong immunostaining with a mottled appearance. Both control and experimental groups show that BSP is absent in PDL region. This is in accordance with immunolocalization results reported by McKee and Nanci [Ref Cooper et al., 2006]. From polarized microscopic images, the birefringence is more prominent in the cementum–PDL interface and alveolar bone, suggesting the presence of many well aligned collagen fibers. Some birefringence is also noticed in the newly formed bone region for experimental group, indicating strain-mediated modeling process of the bone when subject to strain. These observations suggest strain prompt new bone formation from alveolar bone region at the PDL–bone interface. Enclosed boxes in panels a1 and b1 represent regions, which are tension dominating and shown at higher magnification in panels a2 and b2. Panels a3 and b3 are correspondent to a2 and b2 respectively, when analyzer and polarizer are applied. AB: alveolar bone, PDL: periodontal ligament, C: cementum, NB: new bone, V: blood vessel.
Mentions: The distribution of BSP was mainly associated with mineralized regions of the tissue such as cementum and alveolar bone as well as newly formed bony protrusions (Fig. 3). BSP was absent in the PDL. The light brown color in the new bone (NB, Fig. 3b2) indicated a lower content of BSP, suggesting an early stage of BSP deposition among other matrix proteins (Fig. 3e). A strong immunostaining was observed in the cementum and alveolar bone, as indicated by the darker brown, suggesting that these mineralized regions could be mature in terms of matrix protein deposition (Fig. 3). Birefringence using polarized light indicated well-aligned collagen fibers at specific regions such as the PDL–cementum and PDL–bone interfaces (Fig. 3a3 and b3). The birefringence in the new bone region is sparse, suggesting that the collagen fibers do not have the same extent of organization (Fig. 3b3). This is consistent with the results obtained from PSR staining (Fig. 2g and h).

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