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Etiology and pathogenesis of periodontal disease

Introduction

While there are many factors associated with the development of periodontal disease, the inciting etiologic agent is plaque bacteria.1–8 Research has shown that inflammation will continue as long as the gingiva is exposed to a bacterial biofilm and will resolve after its removal.9,10 In fact, one author emphatically states, “Forty years of experimental research, clinical trials, and demonstration projects in different geographical and social settings have confirmed that effective removal of dental plaque is essential to dental and periodontal health throughout life.”11

Periodontal disease is described in two stages, gingivitis and periodontitis. Gingivitis is the initial, reversible stage of the disease process in which the inflammation is confined to the gingival tissues.6,12 In other words, there is no inflammation involving the periodontal ligament or alveolar bone. The gingival inflammation, which is initiated by plaque bacteria, may be reversed with a thorough dental prophylaxis and consistent homecare.12,13

Periodontitis is the later stage of the disease process and is defined as an inflammatory disease of the deeper supporting structures of the tooth (periodontal ligament and alveolar bone) caused by microorganisms.3,14 These conditions are discussed in detail in respective chapters. This chapter will focus on the pathogenesis of both of these diseases, which are often interrelated.

Plaque

Periodontal disease (both gingivitis and periodontitis) is initiated when oral bacteria adhere to the teeth in a substance called plaque.1,2,6,10,15 Dental plaque is defined as a structured, resilient substance that adheres tenaciously to intraoral hard tissues.15–17 Plaque is a biofilm which is made up almost entirely of oral bacteria, contained in a matrix composed of salivary glycoproteins and extracellular polysaccharides.6,15,17,18 A biofilm is a unique environment in which nutrients (as well as oxygen) diffuse through the different layers, which supports changes in microbiotic composition.15 In addition, there exists a series of fluid channels within the plaque biofilm that facilitate nutrient delivery and waste removal.18,19 As such, these channels act as a primitive circulatory system for the biofilm. In essence, plaque is a unique organism.18

Adherence of plaque

The warm, moist, nutrient-rich environment of the oral cavity makes it an ideal breeding ground for bacteria. Fortunately, many of these bacteria are swallowed or “drooled” and therefore do not contribute to periodontal disease. For bacteria to initiate periodontal disease, they must remain attached to the oral tissues, and therefore adherence is an important aspect of periodontal disease. There are several niches for this to occur within the mouth, including the teeth, periodontium, buccal ­epithelium, tongue, and tonsils.15 The first two are most important in the discussion of periodontal disease.

Although the periodontium is easily colonized by oral bacteria, there appears to be individual variation between animals as to the relative adherence of bacteria. In fact, it has been shown that bacterial adherence is increased in those who are predisposed to periodontal disease.20 Fortunately, the high turnover rate of the oral soft tissues limits the level of infection.

The major niche for bacterial colonization is the teeth.15 Teeth are particularly prone to bacterial adherence because they are hard, irregular, and non-shedding. They also create a unique and abrupt transition from the periodontal tissues. The combination of these factors makes the teeth very efficient bacterial colonization sites. Plaque adherence is further enhanced by many anatomic or pathologic states that may either roughen the teeth or inhibit plaque removal.15,21 Factors associated with a roughened tooth surface include enamel hypocalcification (Figure 2.1), tooth resorption or uncomplicated crown fractures (Figure 2.2), wear (attrition or abrasion) (Figure 2.3), or presence of calculus.3 Conditions that inhibit plaque removal (normally achieved by either natural means such as chewing or by homecare methods) include crowding (Figure 2.4), periodontal pockets (Figure 2.5), gingival foreign bodies (Figure 2.6), or gingival hyperplasia (Figure 2.7).3 Therefore, these issues should be addressed along with standard periodontal care. Additionally, gingival inflammation has been shown to increase plaque accumulation22 (likely due to increased crevicular fluid production and the nutrients it supplies).15 This finding proves the critical importance of good oral hygiene.

Figure 2.1 Intraoral picture of the maxillary left of a dog with widespread enamel hypocalcification. Note the significant calculus and gingival inflammation on the canine (white arrows), especially when compared with the second incisor and first premolars (blue arrows), which are unaffected.

Plaque formation

The process of plaque formation is divided into three major stages: formation of the pellicle, initial bacterial adhesion and attachment, and finally bacterial colonization and plaque maturation.15

The first stage is formation of the pellicle on the surface of the teeth, which starts within nanosoeconds of a prophylaxis.15 The pellicle is a thin, saliva-derived layer including numerous proteins (such as glycoproteins), enzymes, and other molecules that act as attachment sites for bacteria.6 The initial pellicle differs from saliva and therefore is thought to form by selective adsorption of macromolecules. The physical and chemical nature of the underlying surface significantly affects the properties of the pellicle.23,24 In addition, these characteristics can be transferred through the pellicle layer and continue to affect bacterial adhesion.25 Therefore, the surfaces of the teeth have a significant influence on the formation of plaque.

Figure 2.2 (a) Intraoral dental picture of a feline patient with tooth resorption and associated calculus. This has contributed to the periodontal loss as demonstrated by the probe. (b) Intraoral picture of the left maxillary fourth premolar (208) of a dog that has an uncomplicated crown fracture (blue arrow). Note the significant calculus present (white arrows).

The second stage is the initial adhesion and attachment of bacteria, which occurs within seconds of a prophylaxis.26 This adhesion is not completely understood but can be thought of as occurring in three phases.27 It should be noted that this system is similar to that in all aqueous environments from pipelines to cardiovascular devices. Phase 1 is transportation to the surface of the tooth, which occurs via random contacts, either through Brownian motion, sedimentation, liquid flow, or active bacterial movement (chemotaxis). Phase 2 is the initial adhesion of bacteria through an interaction between the bacteria and the tooth surface, which occurs when the distance separating them is less than 50 nm. The forces responsible for the adhesion can be broken into long- (between 2 and 50 nm) and short-range (< 1 nm) forces. Long-range forces (van der Waals and electrostatic repulsive) typically result in reversible binding. Short-range forces (hydrogen bonding, ion pair formation, steric interaction) do not often come into play (due to the need for a very close association), but when they do, they result in irreversible binding. Phase 3 is true bacterial attachment by specific interactions (covalent, ionic, or hydrogen bonding), which follows direct contact or bridging. This bonding occurs between specific extracellular proteinaceous components (adhesions) on the bacteria and complementary receptors on the pellicle and is species specific.

Figure 2.3 Intraoral picture of the mandibular right of a dog with widespread abrasion (blue arrows). Note the periodontal pocket as well as significant gingival inflammation (white arrows).

It is important to note that bacteria are separated into early and late colonizers. Early colonizers are gram-positive aerobes that bind directly to the pellicle, while secondary colonizers cannot bind to clean tooth surfaces, and thus bind only to the early colonizers.6 Streptococci28 and actinomyces are the typical early colonizers and each bind to specific salivary molecules.29–33 Most of the early colonizing streptococci offer receptor molecules to the oral flora.29

It is critical to note that phase 3 attachment results in irreversible bonding much more readily on rough or irregular surfaces due to the fact that the bacteria are protected from shear forces (see below).

Figure 2.4 (a) Intraoral picture of the maxillary left of a dog with crowding and rotation of the second through fourth premolars (blue arrows) and secondary periodontal disease as evidenced by the gingival recession (white arrows). (b) Intraoral picture of the maxillary right of a dog with crowding and rotation of the second through fourth premolars. Note the significant periodontal loss involving the third premolar (107).

In humans at least, it appears that fusobacterium is a bridge between the early and late colonizers, as the late colonizers appear to coaggregate mostly with it as opposed to directly to early colonizers.34

The final step is colonization and plaque maturation, which is actually a continuation of the initial attachment above. It is initiated when the attached microorganisms multiply and create the microcolonies that make up the...