Читать книгу Biological Mechanisms of Tooth Movement - Группа авторов - Страница 20

Chappin Harris, in 1839, published a book titled The Dental Art, which stated that OTM in the socket depends on resorption and deposition of bone, but it took more than 60 years to have the first histological picture of this phenomenon, which was provided by Carl Sandstedt (Figure 1.8). Sandstedt’s experimental studies of tooth movements in dogs were first published in German in 1901, and later in English (Sandstedt, 1904, 1905). His systematic way of conducting experiments was evident from the incorporation of a control group from the same litter as his two experimental dogs. A sectional fixed appliance was inserted in the upper jaw, which was subjected to repeated activations for palatal tipping of the upper incisors over a three‐week period. Histological sections of the incisor areas were prepared to assess tissue changes. In order to document positional changes of the teeth, plaster casts and radiographs were obtained. With these experiments, he could observe stretching of the periodontal ligament (PDL) in tension sites and narrowing of this tissue in pressure sites. He demonstrated new bone formation in areas of tension, while resorption was observed in areas of compression. In the compressed periodontium, he initially saw signs of necrosis (hyalinization), and described it as “an obviously degenerated product, a hyaline transformation of the connective tissue, in which regenerative processes take place … the old mortified tissue is resorbed and substituted by granulation tissue.” He further noted that “at the limit of the hyaline zone, the alveolar wall presents a deep, undermining notch filled by proliferating cells as in resorptive areas.” Furthermore, “the intensive resorptive process even attacked the incisor itself deeply into the dentine,” and he assumed that this process is a common secondary effect of OTM. Figure 1.9 is a photograph of a cross section of a premolar root, showing areas of necrosis in the PDL, as well as multiple osteoclasts in Howship’s lacunae at the PDL–alveolar bone interface. These cells were, in Sandsted’s opinion, the main cells responsible for force‐induced tooth movement (Persson, 2005; Bister and Meikle, 2013).

He ended his landmark article by proposing a role for bone bending in the tooth movement process in line with the thinking provided by Kingsley and Farrar.

In 1911/1912, Oppenheim reported that tooth‐moving forces caused complete transformation (remodeling) of the entire alveolar process, indicating that orthodontic force effects spread beyond the limits of the PDL. E.H. Angle, the father of modern orthodontics, invited Oppenheim to lecture to his students, who accepted Oppenheim’s hypothesis enthusiastically. Oppenheim, the proponent of “the law of bone transformation,” rejected both the pressure/tension hypothesis supported by the histological evidence of Sandstedt, and the theory of bone bending hypothesis advanced by Kingsley and Farrar, based on the elastic properties of bone. Oppenheim’s experiments were conducted on mandibular deciduous incisors of baboons (the number of animals he used and the appliances he used remain ambiguous) and suggested that only very light forces evoke the required tissue responses. He stated that an increase in the force levels will produce occlusion of the vascular supply, as well as damage to the PDL and the other supporting tissues, and that the tooth will act as a one‐armed lever when light forces were applied, and like a two‐armed lever during the application of heavy forces. He also demonstrated how alveolar bone is restored structurally and functionally during the retention period (Noyes, 1945). As a proponent of bone transformation and Wolff ’s law, Oppenheim received acceptance from Angle, as it supported his thoughts in the matter. Oppenheim was also supported by Noyes, one of Angle’s followers and an established histologist.

Figure 1.8 Carl Sandstedt (1860–1904), the father of biology of orthodontic tooth movement.

Figure 1.9 A figure from Carl Sandstedt’s historical article in 1904, presenting a histological picture of a dog premolar in cross section, showing the site of PDL compression, including an osteoclastic front and necrotic (hyalinized) areas.

Oppenheim’s research highlighted common concepts, shared by orthodontists and orthopedists, who were convinced that both specialties should be based upon a thorough knowledge of bone biology, particularly in relation to mechanical forces and their cellular reactions. However, it became evident that in orthodontics the PDL, in addition to bone, is a key tissue with regards to OTM.

Working on Macacus rhesus monkeys in 1926, Johnson, Appleton, and Rittershofer reported the first experiment where they recorded the relationship between the magnitude of the applied force and the distance in which it was active. In 1930, Grubrich reported surface resorptions in teeth subjected to orthodontic forces, a finding confirmed by Gruber in 1931. Even before these histological observations of surface changes were reported, Ketcham (Figure 1.10) (1927, 1929) presented, radiographic evidence that root resorption may result from the application of faulty mechanics and the existence of some unknown systemic factors. Schwarz (1932) conducted extensive experiments on premolars in dogs, using known force levels for each tooth. The effects of orthodontic force magnitude on the dog’s paradental tissue responses were examined with light microscopy. Schwarz classified orthodontic forces into four degrees of biological efficiency:

Figure 1.10 Albert Ketcham (1870–1935), who presented the first radiographic evidence of root resorption. He was also instrumental in forming the American Board of Orthodontics.

(Source: Siersma, 2015. Reproduced with permission of Elsevier.)

 below threshold stimulus;

 most favorable – about 20 g/cm2 of root surface, where no injury to the PDL is observed;

 medium strength, which stops the PDL blood flow, but with no crushing of tissues;

 very high forces, capable of crushing the tissues, causing irreparable damage.

He concluded that an optimal force is smaller in magnitude than that capable of occluding PDL capillaries. Occlusion of these blood vessels, he reasoned, would lead to necrosis of surrounding tissues, which would be harmful, and would slow down the velocity of tooth movement.

The proposed optimal orthodontic force concept by Schwartz was supported by Reitan (Figure 1.11), who conducted thorough histological examinations of paradental tissues incidental to tooth movement. Reitan’s studies were conducted on a variety of species, including rodents, canines, primates, and humans, and the results were published during the period from the 1940s to the 1970s. Figure 1.12 displays the appearance of an unstressed PDL of a cat maxillary canine. The cells are equally distributed along the ligament, surrounding small blood vessels. Both the alveolar bone and the canine appear intact. In contrast, the compressed PDL of a cat maxillary canine that had been tipped distally for 28 days, with an 80 g force (Figure 1.13), appears very stormy. The PDL near the root is necrotic, but the alveolar bone and PDL at the edge of the hyalinized zone are being invaded by cells that appear to remove the necrotic tissue, as evidenced by a large area where undermining resorption has taken place. Figure 1.14 shows the mesial side of the same root, where tension prevails in the PDL. Here the cells appear busy producing new trabeculae arising from the alveolar bone surface, in an effort to keep pace with the moving root. To achieve this type of tissue and cellular responses to orthodontic loads, Reitan favored the use of light intermittent forces, because they cause minimal amounts of tissue damage and cell death. He noted that the nature of tissue response differs from species to species, reducing the value of extrapolations.

Figure 1.11 Kaare Reitan (1903–2000), who conducted thorough histological examinations of paradental tissues.

Figure 1.12 A 6 μm sagittal section of a frozen, unfixed, nondemineralized cat maxillary canine, stained with hematoxylin and eosin. This canine was not treated orthodontically (control). The PDL is situated between the canine root (left) and the alveolar bone (right). Most cells appear to have an ovoid shape.

Figure 1.13 A 6 μm sagittal section of a cat maxillary canine, after 28 days of application of 80 g force. The maxilla was fixed and demineralized. The canine root (right) appears to be intact, but the adjacent alveolar bone is undergoing extensive resorption, and the compressed, hyalinized PDL is being invaded by cells from neighboring viable tissues (fibroblasts and immune cells). H & E staining.

Figure 1.14 The mesial (PDL tension) side of the tooth shown in Figure 1.13. Here, new trabeculae protrude from the alveolar bone surface, apparently growing towards the distal‐moving root. H & E staining.

With experiments on human teeth, Reitan observed that tissue reactions can vary, depending upon the type of force application, the nature of the mechanical design, and the physiological constrains of the individual patient. He observed the appearance of hyalinized areas in the compressed PDL almost immediately after continuous force application and the removal of those hyalinized areas after 2–4 weeks. Furthermore, Reitan reported that in dogs, the PDL of rotated incisors assumes a normal appearance after 28 days of retention, while the supracrestal collagen fibers remain stretched even after a retention period of 232 days. Consequently, he recommended severing the latter fibers surgically. He also called attention to the role of factors such as gender, age, and type of alveolar bone, in determining the nature of the clinical response to orthodontic forces. He also reported that 50 g of force is ideal for movement of human premolars, resulting from direct resorption of the alveolar bone.

Another outlook on differential orthodontic forces was proposed by Storey (1973). Based upon experiments in rodents, he classified orthodontic forces as being bioelastic, bioplastic, and biodisruptive, moving from light to heavy. He also reported that in all categories, some tissue damage must occur in order to promote a cellular response, and that inflammation starts in paradental tissues right after the application of orthodontic forces.

Continuing the legacy of Sandstedt, Kvam and Rygh studied cellular reactions in the compression side of the PDL. Rygh (1974, 1976) reported on ultrastructural changes in blood vessels in both human and rat material as packing of erythrocytes in dilated blood vessels within 30 minutes, fragmentation of erythrocytes after 2–3 hours, and disintegration of blood vessel walls and extravasation of their contents after 1–7 days. He also observed necrotic changes in PDL fibroblasts, including dilatation of the endoplasmic reticulum and mitochondrial swelling within 30 minutes, followed by rupture of the cell membrane and nuclear fragmentation after 2 hours; cellular and nuclear fragments remained within hyalinized zones for several days. Root resorption associated with the removal of the hyalinized tissue was reported by Kvam and Rygh. This occurrence was confirmed by a scanning electron microscopic study of premolar root surfaces after application of a 50 g force in a lateral direction (Kvam, 1972). Using transmission electron microscopy (TEM), the participation of blood‐borne cells in the remodeling of the mechanically stressed PDL was confirmed by Rygh and Selvig (1973), and Rygh (1974, 1976). In rodents, they detected macrophages at the edge of the hyalinized zone, invading the necrotic PDL, phagocytizing its cellular debris and strained matrix.

After direct measurements of teeth subjected to intrusive forces, Bien (1966) hypothesized that there are three distinct but interacting fluid systems involved in the response of the PDL to mechanical loading: the fluids in the vascular network, in the cells and fibers, and the interstitial fluid. Mechanical loading moves fluids into the vascular reservoir of the marrow space through the many minute perforations in the tooth alveolar wall. The hydrodynamic damping coefficient (Figure 1.15) is time dependent, and therefore the damping rate is determined by the size and number of these perforations. As a momentary effect, the fluid that is trapped between the tooth and the socket tends to move to the boundaries of the film at the neck of the tooth and the apex, while acting to cushion the load and is referred to as the “squeeze film effect”. As the squeeze film is depleted, the second damping effect occurs after exhaustion of the extracellular fluid, and the ordinarily slack fibers tighten. When a tooth is intruded, the randomly oriented periodontal fibers, which crisscross the blood vessels, tighten, then compress and constrict the vessels that run between them, causing stenosis and ballooning of the blood vessels, creating a back pressure. Thus, high hydrodynamic pressure heads can be created suddenly in the vessels above the stenosis. At the stenosis, a drop of pressure would occur in the vessel in accordance with Bernoulli’s principle that the pressure in the region of the constriction will be less than elsewhere in the system. Bien also differentiated the varied responses obtained from momentary forces of mastication from that of prolonged forces applied in orthodontic mechanics and suggested that biting forces in the range of 1500 g/cm² will not crush the PDL or produce bone responses.

Figure 1.15 The constriction of a blood vessel by the periodontal fibers. The flow of blood in the vessels is occluded by the entwining periodontal fibers. Below the stenosis, the pressure drop gives rise to the formation of minute gas bubbles, which can diffuse through the vessel walls. Above the stenosis, fluid diffuses through the walls of the cirsoid aneurysms formed by the build‐up of pressure.

(Source: Bien, 1966. Reproduced with permission of SAGE Publications.)

Pointing out a conceptual flaw in the pressure tension hypothesis proposed by Schwarz (1932), Baumrind (1969) concluded from an experiment on rodents that the PDL is a continuous hydrodynamic system, and any force applied to it will be transmitted equally to all regions, in accordance with Pascal’s law. He stated that OTM cannot be considered as a PDL phenomenon alone, but that bending of the alveolar bone, PDL, and tooth is also essential. This report renewed interest in the role of bone bending in OTM, as reflected by Picton (1965) and Grimm (1972). The measurement of stress‐generated electrical signals from dog mandibles after mechanical force application by Gillooly et al. (1968), and measurements of electrical potentials, revealed that increasing bone concavity is associated with electronegativity and bone formation, whereas increasing convexity is associated with electropositivity and bone resorption (Bassett and Becker, 1962). These findings led Zengo et al. (1973) to suggest that electrical potentials are responsible for bone formation as well as resorption after orthodontic force application. This hypothesis gained initial wide attention but its importance diminished subsequently, along with the expansion of new knowledge about cell–cell and cell–matrix interactions, and the role of a variety of molecules, such as cytokines and growth factors in the cellular response to physical stimuli, like mechanical forces, heat, light, and electrical currents.