Biomechanics of Oral Collagenous Soft Tissues and their Roles in Mechanobiological Processes and Clinical Implications

Abstract

Biomechanical properties are central to the functions of many oral soft tissues, which are determined by the hierarchical organisation of their constituents. External mechanical stimulation is sensed by the cellular components of these soft tissues. In response, they adapt their own structures and simultaneously regulate turnovers of the neighbouring hard tissues across multiple length scales. Consequently, they alter the biomechanical behaviours of the tissue complex to achieve improved functionality or minimise further damage. Periodontal ligament (PDL) and alveolar mucosa (AM) in the oral cavity are two typical examples, and the adaptation processes driven by them have been considered and exploited in clinical applications. Both PDL and AM are collagenous tissues rich in interstitial fluid. Recent studies have shown that the interstitial fluid pressure (IFP) acts as a key factor in driving the mechanobiological processes. In orthodontic tooth alignment, IFP drives the remodelling of alveolar sockets therefore allowing the teeth to move. In prosthodontic denture treatment, IFP induces residual ridge resorption often causing ill-fitting of the prosthesis over time.

Despite positive correlations reported between IFP in these two soft tissues and the turnover of their adjacent hard tissues, there are many unanswered questions, including two investigated in this PhD thesis. First is the microscopic heterogeneity of biomechanical properties and mechanobiological responses. For PDL-driven tooth movement, the location and amount of bone remodelling and root resorption were reported with a significant heterogeneity on a microscopic scale, including the candidate’s MPhil study. Thus, it is hypothesized that the organisation of the constituents in these tissues, especially the collagen network, leads to a heterogenous distribution of stimulation to cells. Such microstructural or mechanical heterogeneity has not yet been quantitatively characterised in the PDL. Second is the mechanobiological responses over a time frame relevant to a treatment course. In the AM-driven mandibular residual ridge resorption beneath a denture, the magnitude of IFP was found to decay over time as bone resorption occurred. A nonlinear trajectory was proposed in this time-dependent process, but a quantitative relationship between IFP and resorption has been hindered by the lack of long-term clinical data until recently.

To tackle these questions, this thesis aimed to develop two frameworks, 1) to quantify the collagen network architecture and its effect on tissue mechanics by considering the PDL; and 2) to simulate bone remodelling driven by AM under overdentures over time. Both frameworks integrated a variety of imaging techniques, advanced image segmentation and quantification techniques, finite element simulation, and in-house developed algorithms. The combination of experimental and computational approaches allows deciphering of the basic governing principles behind the structure-mechanics-adaptation relationships of these tissues across multiple length scales. The knowledge will contribute to optimising treatment plans, predicting the trajectory of pathological processes, and developing new bio-templates for regenerative medicine. More importantly, both frameworks can be directly applied to a wide range of soft tissues for studying their biomechanics-centred functionality and dysfunction.