The tooth attachment mechanism defined by structure, chemical composition and mechanical properties of collagen fibers in the periodontium

Abstract

In this study, a comparison between structure, chemical composition and mechanical properties of collagen fibers at three regions within a human periodontium, has enabled us to define a novel tooth attachment mechanism. The three regions include, (1) the enthesis region: insertion site of periodontal ligament (PDL) fibers (collagen fibers) into cementum at the root surface, (2) bulk cementum, and (3) the cementum-dentin junction (CDJ). Structurally, continuity in collagen fibers was observed from the enthesis, through bulk cementum and CDJ. At the CDJ the collagen fibers split into individual collagen fibrils and intermingled with the extracellular matrix of mantle dentin. Under wet conditions, the collagen fibers at the three regions exhibited significant swelling suggesting a composition rich in polyanionic molecules such as glycosaminoglycans. Additionally, site-specific indentation illustrated a comparable elastic modulus between collagen fibers at the enthesis (1-3 GPa) and the CDJ (2-4 GPa). However, the elastic modulus of collagen fibers within bulk cementum was higher (4-7 GPa) suggesting presence of extrafibrillar mineral. It is known that the tooth forms a fibrous joint with the alveolar bone, which is termed a gomphosis. Although narrower in width than the PDL space, the hygroscopic CDJ can also be termed as a gomphosis; a fibrous joint between cementum and root dentin capable of accommodating functional loads similar to that between cementum and alveolar bone. From an engineering perspective, it is proposed that a tooth contains two fibrous joints that accommodate the masticatory cyclic loads. These joints are defined by the attachment of dissimilar materials via graded stiffness interfaces, such as: (1) alveolar bone attached to cementum with the PDL; and (2) cementum to root dentin with the CDJ. Thus, through variations in concentrations of basic constituents, distinct regions with characteristic structures and graded properties allow for attachment and the load bearing characteristics of a tooth.

Figure 1

Structure of cementum; a-d) Polarized microscopy; a) demineralized section stained with Safranin O counterstained with fast green. Notice the continuous collagen fibers from the root surface to root mantle dentin (segmented curved arrows). a and b) Notice tufts of collagen fibers between lamellar cementum and mantle dentin (stars) form the hydrophilic CDJ. c and d) a demineralized section stained with Masson’s trichrome. Notice the two distinct orientations of collagen fibers; radial collagen fibers (PDL-inserts) or Sharpey’s fibers perpendicular (segmented arrows) to the circumferential or lamellar collagen fibers. e) 100 μm × 100 μm AFM micrograph from dry ultrasectioned surface-block specimen. Notice the 5 μm wide collagen fibers from the root surface through the CDJ into mantle dentin (segmented white arrow). The CDJ is a valley-like under dry conditions.

Figure 2

a) A demineralized section stained with Masson’s trichrome illustrating integration of terminal ends of the radial collagen fibers (PDL-inserts) with root mantle dentin. The exclusively radial collagen fiber rich region representative of CDJ is 20 μm wide. b) An AFM micrograph of undemineralized cementum illustrating similar termini of collagen fibers (stars). Note the radial and circumferential collagen fibers within bulk cementum. c1, 2 and 3). An AFM micrograph showing web-like PDL termini at the mantle dentin and intermingling of the 200 nm wide collagen fibrils with the extracellular matrix.

Figure 3

A composite of AFM micrographs of a wet ultramicrotomed surface-block. This image illustrates two distinct fibrous regions with corresponding ranges for modulus values; 1) enthesis and 2) the interface between cementum and root dentin (CDJ), illustrating ligament-like collagen fibers within bulk cementum extending into root mantle dentin.

Figure 4

a) AFM deflection images in contact mode showing collagen fibrils (arrows) within undemineralized cementum. Notice collagen fibrils from adjacent cementum crossing over the lower fibrils at almost 90°. b) Notice the periodic pattern of the collagen fibrils (stars) with the collagen fiber. The absence of the periodic pattern of the collagen fibril (arrows) could be due to a coating of noncollagenous proteins and/or extrafibrillar mineral. Note: The fibrils shown in this figure are within a valley-like region. The regions represented by triangles are walls of the valley. It should be noted that the topography of the valley-walls could be an image artifact caused by specimen-surface and tip-geometry limitations [22].

Figure 5

Schematic (not to scale) of the tissues and the interfaces responsible for tooth attachment illustrating the a) observed structure and b) variation in elastic modulus across alveolar bone, PDL, cementum and root dentin. The values for the PDL are from Cattaneo et al., 2005 [21], while the values for other materials were based on those observed in our laboratory. The wide range in elastic modulus is due to the viscoelastic nature of the fibrous PDL. Distinct regions with characteristic structures and graded properties allow for attachment and the load bearing characteristics of a tooth.

Figure 6

A detail schematic (not to scale) illustrating the macroscale root of a tooth and the microscale regions involved in tooth attachment. The distinct microscale regions are shown from left to right a) light micrograph of circumferential and radial collagen fibers within bulk cementum, b) AFM micrograph illustrating hydrated PDL-inserts (collagen fiber) within bulk cementum, c) light micrograph illustrating the CDJ formed by collagen fibrils, d) an AFM micrograph illustrating hydrated CDJ and collagen fibers.