Several different theories on the aetiology of dental caries have been proposed, but it is generally accepted that it is primarily caused by acidogenic micro-organisms converting fermentable carbohydrates to acids. There is still some discussion on whether caries is caused by specific micro-organisms or a non-specific mix of different micro-organisms and on whether caries is a classical infection or is caused by dysregulation of the normal oral bacteria (dysbiosis). Two types of dental caries are recognised in horses, i.e. peripheral dental caries and infundibular dental caries, with peripheral caries appearing to be increasingly recognised. Little is known about the prevalence and severity of peripheral dental caries in the general equine population, or the risk factors and micro-organisms involved in its aetiopathogenesis. Limited pathological studies have shown two types of cemental destruction in equine peripheral caries, and indicate that gross dental examination underestimates the severity of equine peripheral caries.
Dental caries is defined as a demineralisation of the calcified (inorganic) dental tissues and a destruction of its organic component (Soames and Southam, 2005). The aetiopathogenesis of equine dental caries (both infundibular and peripheral) are poorly understood, although some prevalence surveys and limited pathological and conventional bacteriological studies have been performed on these disorders.
In contrast, dental caries in humans, and in brachydont (short-crowned teeth) animals (often as models for human dentistry) have been well studied and consequently this literature review is mainly based on brachydont dental studies. Although incisors also have infundibulae, infundibular caries has only been described in maxillary cheek teeth. Peripheral caries can affect all teeth, but is very rare in canine or incisor teeth.
Chemoparasitic or Acidogenic Theory
Miller (1889) was first to propose bacterial involvement in the development of dental caries in the acidogenic theory of caries. He postulated that dietary carbohydrates were fermented by oral micro-organisms into acids, primarily lactic acid, but also acetic and propionic acid. These acids caused a drop in the pH of dental plaque and when it decreases below the critical level of 5.5, mineral ions are released from the hydroxyapatite crystals of enamel, initiating caries.
The same occurs in cementum at a less acidic level, i.e. at a pH level of 6.7 (Tanzer, 1992), whereas the critical pH in dentine is about 6.0 (Vanusprong et al., 2002). The opposite effect also occurs, i.e. teeth become remineralised when the pH increases above the critical value (Soames and Southam, 2005). However, these critical pH levels are not rigid, because the process of demineralisation/remineralisation also depends on the levels of hydroxyl, phosphate and calcium ions in plaque fluid and saliva (Dawes, 2003). The higher these hydroxyl, phosphate and calcium levels are in the fluid surrounding the teeth, the lower the critical pH will be. Because the concentrations of these ions in saliva and plaque fluid can vary between individuals, the critical pH levels can also vary accordingly. With demineralistion of teeth, bacterial destruction of the now-exposed proteins and other organic components of dental tissues also occur (Soames and Southam 2005). Previously, Gottlieb (1944) postulated in the proteolytic theory of caries that proteolysis of the organic matrix precedes the disintegration of inorganic components in caries development, with their organic matrix, like enamel lamellae and rods forming a pathway for the invasion of microorganisms. Later, Martin et al. (1955) proposed a simultaneous microbial degradation of organic components (proteolysis) and dissolution of minerals of the tooth by the process of chelation in the proteolysis-chelation theory. They suggested that the breakdown products of organic components have chelating properties and dissolved the minerals in the tooth. Current evidence favours the acidogenic theory initially proposed by Miller (1989).
Caries must be differentiated from dental erosion which is caused by the direct action of acids on teeth by dissolving exposed calcified dental surfaces (cementum, enamel and/or dentine). Dental erosion occurs over a larger dental area compared to caries and without the need for bacteria. An erosive (i.e. acidic) agent is a greater challenge for an exposed dental surface than a cariogenic substrate (i.e. fermentable carbohydrates) since an erosive agent usually contains no or low levels of calcium and phosphate, while the milieu of an acidic plaque is partly saturated with these ions. Moreover, the rate of demineralisation of an exposed dental surface due to an erosive substance is higher than that caused by a caries process, since in the former, calcium and phosphate ions which become dissolved are detached from the dental surface very quickly and immediately lost, whereas in caries, the dissolved minerals are transported away from the tooth more slowly partly because of the overlying plaque (Shellis, 2013). In horses, widespread dental erosion has been recorded in horses fed abnormally acidic silage (haylage) (Dixon et al., 2010).
Prerequisites for development of caries
The prerequisites for a dental caries lesion to develop are: tooth, substrate, plaque and bacteria (Keyes, 1960). Because the environment of the tooth surface beneath plaque is largely anaerobic, the subsequent anaerobic metabolism of carbohydrates by plaque bacteria will preferentially produce acids. Although factors such as location, composition and morphology of the tooth may also play a role in the development of caries, caries will not develop without the presence of acidogenic bacteria and substrate (monosaccharides, disaccharides or other fermentable carbohydrates).
The pH changes that occur on exposed dental surfaces in response to ingestion of fermentable dietary carbohydrates are similar in teeth with and without caries. However, the initial pH in the plaque overlying teeth suffering from caries is lower and therefore the pH will remain under the critical level for a longer period than occurs beneath the pellicle of healthy teeth (Soames and Southam, 2005). The frequency of fermentable carbohydrate intake is also important in the pH cycling of plaque (Fig 1). The more frequently that fermentable carbohydrates are ingested, the longer the plaque will be below the critical pH and thus will result in a tilting of the balance between demineralisation and remineralisation towards demineralisation (Ten Cate, 2015). It has been suggested that frequent feeding of high levels of concentrates to horses, may predispose to peripheral caries (Dixon et al., 2010), which is supported by the acidogenic theory. Horses trickle feed for up to 18 hours per day, primarily on forage, and if such forage contains simple carbohydrates, such as fructans that occurs in young grass, there is great potential to maintain a critical pH in their oral cavity for prolonged periods.
Fig 1: The pH cycling in human dental plaque depends on the frequency of fermentable carbohydrate intake: (a) eating three times a day; (b) eating six times a day and (c) eating nine times a day. The arrows indicate the time of food intake. The broken red lines represents the critical pH under which demineralisation occurs and above which remineralisation can occur (adapted from Ten Cate, 2015).
Pellicle, plaque and bacteria
The normal thin biofilm adherent to the surface of the teeth is termed a pellicle (acquired pellicle), but if this biofilm becomes very thick and of abnormal composition, it is termed a plaque, whose presence is one of the prerequisites for caries development. Normal pellicle formation starts within seconds of a tooth being exposed to saliva and plays an important role in oral lubrication, regulation of mineral homeostasis and host defense (Siquera et al, 2012). The pellicle is a thin (0.5-1µm), largely proteinaceous layer, containing some carbohydrates and lipids that form on the surface of normal teeth. The sources of these compounds are salivary secretions, gingival crevicular fluid, oral epithelial cell and oral microbial products (Hannig and Joiner, 2006; Siquera et al, 2012). Bacteria can adhere to acquired pellicle within three minutes of exposure of teeth to saliva (Hannig et al., 2007) and the proteins in pellicle have specific receptors for bacterial adhesins that facilitate this process (Douglas, 1994; Hannig et al, 2007).
Plaque is an abnormal, thick biofilm that mainly consists of an organic matrix of salivary mucins (mucopolysaccharides, the major glycoprotein components of mucus) and extracellular polysaccharide polymers with attached micro-organisms (Soames and Southam, 2005). As the plaque biofilm matures, its microbial community becomes more complex (Fig 2). The rate of growth of dental plaque depends on the availability of nutrients, competition with other micro-organisms, and environmental conditions within the biofilm (Chávez de Paz et al., 2008). Predilection sites for plaque to accumulate include mechanically protected areas (Buchalla, 2013) and this would also appear to be the case in horses, as plaque is frequently found in cheek teeth diastemata (Cox et al., 2012). In humans, the microbial community of the supragingival plaque differs from that of the subgingival plaque (Costalonga and Herzberg, 2014). Erridge et al. (2012) used a thickness of 10 µm to distinguish pellicle from plaque in an equine dental peripheral caries study.
Supragingival plaque can have a structured architecture with polymere-containing channels or (“black holes”) connecting the dental surface with the oral cavity (Auschill et al., 2001; Marsh, 2005). The micro-organisms in this biofilm have an uneven spatial arrangement (Auschill et al., 2001), with the most viable bacteria present in the central part of the plaque and lining the channels where diffusion of nutrients takes place. Dead bacteria surrounding the viable bacteria were found closest to the tooth surface and the oral cavity and may function to protect the underlying, living micro-organisms (Auschill et al., 2001).