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

• Load-mediated shifts in mechanical strains will prompt self-governing zones at PDL-cementum and PDL-bone entheses.
• The intensity of strain amplification is predominantly felt at the entheses as it is a region where disparate materials attach.
• Physicochemical observations at the PDL-bone enthesial zone are not directly correlated to the events at PDL-cementum zone.
• Rapid shifts in PDL strain can prompt a shift in mineral apposition at respective entheses albeit of an adapted quality.

ObjectiveThe 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.DesignAccentuated 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.ResultsUnique 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.ConclusionsFrom 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.

Biomineralization can be prompted by differentiating zones along the strained fibers of the periodontal ligament (PDL), specifically at the PDL–bone functional attachment site in a bone–PDL–tooth fibrous joint.  This hypothesis was investigated in vivo by using a rat model and exploiting the fundamental principle, that eccentric loads accentuate strains specifically at regions where dissimilar materials are attached.Figure optionsDownload as PowerPoint slideStrain-guided biomineralization was induced by applying a unidirectional force on molars in a rat in vivo model. Associated changes in PDL-space, biomineralization, and resorption profiles along the PDL fibers and cementum were recorded following the application of a 0.06 N force for 14 days. Vectorial biomineralization identified as finger-like bony protrusions from the highly adaptive and semi-autonomous PDL–bone interface, was identified via micro-X-ray computed tomography (micro-XCT), and dynamic histomorphometry, and was correlated with osteoclast distribution detected by tartrate-resistant acid phosphatase (TRAP) staining. Unique chemical and mechanical qualities including the hygroscopic Sharpey's finger inserts contributing to a higher organic (amide III-1240 cm− 1) to inorganic (phosphate-960 cm− 1) ratio, and a lower elastic modulus of 8 GPa versus 12 GPa for primary bone regions identified by using atomic force microscopy (AFM), nanoindentation, and Raman spectroscopy. Furthermore, an increased presence of elemental Zn in cement lines and mineralized fronts was observed. Adapted regions that were predominantly woven bone and rich in biglycan (BGN) also contained large-molecular weight polysaccharides at the mineralizing front. 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.