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

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

Tension-dominating regions in control groups and experimental groups showing hematoxylin and eosin (H&E) staining (a–d), picrosirius red (PSR) staining visualized under polarized light microscope (e–h), alcian blue counterstained with nuclear fast red (AB-NFR) (i–l), and immunohistochemistry for biglycan (BGN) (m–p). These are all tension-dominating regions, that is, mesial side of maxillary second molar in control groups and distal side of maxillary second molar in experimental groups. Bone–PDL interface in control group is smooth, well-demarcated and highly-birefringent (a, b), whereas experimental group shows finger-like bone protrusions (white arrows in panels of c, d), which is correspondent to the greenish-orange colored bone adjacent to the bone–PDL interface (g, h). In the control group, high birefringence of collagen is shown both at bone–PDL and cementum–PDL interfaces indicating the existence of well-organized Sharpey's fibers (e, f). In the experimental group, however, collagen fibers appear to be more stretched but they show poor quality of organization at bone–PDL interface and the alveolar bone adjacent to the interface (indicated by greenish-orange color, enclosed in dotted lines in panels of g, h). AB-NFR staining reveals a layer of acidic polysaccharides-rich zone on the front line of finger-like bone protrusions in experimental group (k, l), which is absent in control group (i, j). BGN is strongly expressed along both bone–PDL and cementum–PDL interfaces in experimental group (black arrows in panels of o, p), but in control group (m, n), BGN is distributed evenly in periodontal ligament and also positive in predentin (asterisk in panel of m). Enclosed boxes in panels a, c, e, g, I, k, m and o (original magnification, × 100) represent regions shown at higher magnification in panels b, d, f, h, j, l, n and p (original magnification, × 200), respectively. Alveolar bone (AB), periodontal ligament (PDL), cementum (C), dentin (D) new bone (NB), and blood vessel (V).
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f0010: Tension-dominating regions in control groups and experimental groups showing hematoxylin and eosin (H&E) staining (a–d), picrosirius red (PSR) staining visualized under polarized light microscope (e–h), alcian blue counterstained with nuclear fast red (AB-NFR) (i–l), and immunohistochemistry for biglycan (BGN) (m–p). These are all tension-dominating regions, that is, mesial side of maxillary second molar in control groups and distal side of maxillary second molar in experimental groups. Bone–PDL interface in control group is smooth, well-demarcated and highly-birefringent (a, b), whereas experimental group shows finger-like bone protrusions (white arrows in panels of c, d), which is correspondent to the greenish-orange colored bone adjacent to the bone–PDL interface (g, h). In the control group, high birefringence of collagen is shown both at bone–PDL and cementum–PDL interfaces indicating the existence of well-organized Sharpey's fibers (e, f). In the experimental group, however, collagen fibers appear to be more stretched but they show poor quality of organization at bone–PDL interface and the alveolar bone adjacent to the interface (indicated by greenish-orange color, enclosed in dotted lines in panels of g, h). AB-NFR staining reveals a layer of acidic polysaccharides-rich zone on the front line of finger-like bone protrusions in experimental group (k, l), which is absent in control group (i, j). BGN is strongly expressed along both bone–PDL and cementum–PDL interfaces in experimental group (black arrows in panels of o, p), but in control group (m, n), BGN is distributed evenly in periodontal ligament and also positive in predentin (asterisk in panel of m). Enclosed boxes in panels a, c, e, g, I, k, m and o (original magnification, × 100) represent regions shown at higher magnification in panels b, d, f, h, j, l, n and p (original magnification, × 200), respectively. Alveolar bone (AB), periodontal ligament (PDL), cementum (C), dentin (D) new bone (NB), and blood vessel (V).

Mentions: Serial sections were stained and analyzed (Fig. 2). The hematoxylin and eosin stain was informative, in that varying cell morphology specifically at the PDL–bone attachment site, including increased capillaries, was observed within the PDL (Fig. S2). At the PDL–bone, there existed a zone of cells with an altered morphology and closer to the commonly known cuboidal shape of osteoblasts (Fig. 2). Additionally, the alternating but irregular layers of bone encroaching the PDL-space (Δ, Δ1, Δ2, Fig. 2c and d) stained pale pink were observed when compared to the existing bone (stars, Fig. 2c and d), and uniform layering in the controls (Fig. 2a and b).


Strain-guided mineralization in the bone – PDL – cementum complex of a rat periodontium
Tension-dominating regions in control groups and experimental groups showing hematoxylin and eosin (H&E) staining (a–d), picrosirius red (PSR) staining visualized under polarized light microscope (e–h), alcian blue counterstained with nuclear fast red (AB-NFR) (i–l), and immunohistochemistry for biglycan (BGN) (m–p). These are all tension-dominating regions, that is, mesial side of maxillary second molar in control groups and distal side of maxillary second molar in experimental groups. Bone–PDL interface in control group is smooth, well-demarcated and highly-birefringent (a, b), whereas experimental group shows finger-like bone protrusions (white arrows in panels of c, d), which is correspondent to the greenish-orange colored bone adjacent to the bone–PDL interface (g, h). In the control group, high birefringence of collagen is shown both at bone–PDL and cementum–PDL interfaces indicating the existence of well-organized Sharpey's fibers (e, f). In the experimental group, however, collagen fibers appear to be more stretched but they show poor quality of organization at bone–PDL interface and the alveolar bone adjacent to the interface (indicated by greenish-orange color, enclosed in dotted lines in panels of g, h). AB-NFR staining reveals a layer of acidic polysaccharides-rich zone on the front line of finger-like bone protrusions in experimental group (k, l), which is absent in control group (i, j). BGN is strongly expressed along both bone–PDL and cementum–PDL interfaces in experimental group (black arrows in panels of o, p), but in control group (m, n), BGN is distributed evenly in periodontal ligament and also positive in predentin (asterisk in panel of m). Enclosed boxes in panels a, c, e, g, I, k, m and o (original magnification, × 100) represent regions shown at higher magnification in panels b, d, f, h, j, l, n and p (original magnification, × 200), respectively. Alveolar bone (AB), periodontal ligament (PDL), cementum (C), dentin (D) new bone (NB), and blood vessel (V).
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4663464&req=5

f0010: Tension-dominating regions in control groups and experimental groups showing hematoxylin and eosin (H&E) staining (a–d), picrosirius red (PSR) staining visualized under polarized light microscope (e–h), alcian blue counterstained with nuclear fast red (AB-NFR) (i–l), and immunohistochemistry for biglycan (BGN) (m–p). These are all tension-dominating regions, that is, mesial side of maxillary second molar in control groups and distal side of maxillary second molar in experimental groups. Bone–PDL interface in control group is smooth, well-demarcated and highly-birefringent (a, b), whereas experimental group shows finger-like bone protrusions (white arrows in panels of c, d), which is correspondent to the greenish-orange colored bone adjacent to the bone–PDL interface (g, h). In the control group, high birefringence of collagen is shown both at bone–PDL and cementum–PDL interfaces indicating the existence of well-organized Sharpey's fibers (e, f). In the experimental group, however, collagen fibers appear to be more stretched but they show poor quality of organization at bone–PDL interface and the alveolar bone adjacent to the interface (indicated by greenish-orange color, enclosed in dotted lines in panels of g, h). AB-NFR staining reveals a layer of acidic polysaccharides-rich zone on the front line of finger-like bone protrusions in experimental group (k, l), which is absent in control group (i, j). BGN is strongly expressed along both bone–PDL and cementum–PDL interfaces in experimental group (black arrows in panels of o, p), but in control group (m, n), BGN is distributed evenly in periodontal ligament and also positive in predentin (asterisk in panel of m). Enclosed boxes in panels a, c, e, g, I, k, m and o (original magnification, × 100) represent regions shown at higher magnification in panels b, d, f, h, j, l, n and p (original magnification, × 200), respectively. Alveolar bone (AB), periodontal ligament (PDL), cementum (C), dentin (D) new bone (NB), and blood vessel (V).
Mentions: Serial sections were stained and analyzed (Fig. 2). The hematoxylin and eosin stain was informative, in that varying cell morphology specifically at the PDL–bone attachment site, including increased capillaries, was observed within the PDL (Fig. S2). At the PDL–bone, there existed a zone of cells with an altered morphology and closer to the commonly known cuboidal shape of osteoblasts (Fig. 2). Additionally, the alternating but irregular layers of bone encroaching the PDL-space (Δ, Δ1, Δ2, Fig. 2c and d) stained pale pink were observed when compared to the existing bone (stars, Fig. 2c and d), and uniform layering in the controls (Fig. 2a and b).

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