The microbial community that forms in plaque has many advantages for the inhabiting micro-organisms (Marsh, 2005). Firstly, pioneer microbial colonisers create a micro-environment that is suitable for the attachment and growth of other micro-organisms, a process termed co-aggregation (Metwalli et al., 2013) (Fig 2). Secondly, molecules that cannot be broken down by individual species of bacteria can often be catabolised by the combination of micro-organisms living in this community. Additionally, a pathogenic synergism may occasionally occur, causing the combination of organisms in the community to be more pathogenic than any of the individual micro-organisms. Furthermore, the collaboration and gene transfer, which are likely to occur in a microbial plaque community, make them more resistant to antimicrobial therapeutics, environmental stress and host defences than oral bacteria living in isolation (Marsh, 2005).
Another survival mechanism that oral bacteria are believed to use is a dormancy state during times of nutrient deprivation, when they enter a state of metabolic arrest without undergoing cell division or growth. This state is also known as a viable but nonculturable state (Oliver, 2010). During this dormant state, bacteria are less sensitive to antimicrobial agents, and also to changes in temperature and pH. When the bacteria later regain access to sufficient nutrients, they return to their higher metabolic rates (metabolic reactivation), with resumption of cell growth and division. A slow reactivation of nutrient-deprived Streptococcus anginosus and Lactobacillus salivarius in oral biofilms after the introduction of nutrients was suggested to also be part of their survival strategy (Chavez de Paz et al. 2008). An enhanced synthesis of certain proteins (that act as stress proteins) by some oral bacteria such as S. mutans may also help these bacteria survive suboptimal conditions (Svensäter et al., 2000).
Micro-organisms involved in human dental caries
The cultivable microbiological flora in dental plaque varies between herbivorous, carnivorous and omnivorous mammalian species, while within the same dietary group, the microflora appears to be quite similar (Dent, 1979). Using molecular bacteriological techniques, the Human Oral Microbiome Database now includes approximately 700 microbial species including bacteria and archaea ( ) that can be present in the human oral cavity in health and disease (Chen et al., 2010).
Although Miller’s acidogenic theory has been generally accepted, there are different theories about which micro-organisms are important in the development of dental caries.
In the specific plaque hypothesis, specific pathogenic micro-organisms are proposed to cause caries. Lactobacilli were initially believed to be the most important bacteria in caries development because of their acidogenic and aciduric characteristics, meaning that they can produce acid and survive in an acidic environment, respectively (Kligler and Gies, 1915; Howe and Hatch, 1917). However, Clarke (1924) discovered a further acidogenic and aciduric bacteria: Streptococcus mutans, which additionally produces extracellular sticky glucans and intracellular polysaccharides. Extracellular sticky glucans enable bacteria to adhere to teeth and intracellular polysaccharides can be converted to acidic end-products, when dietary sugars are absent from the oral cavity (van Loveren, 2012).
A causal relationship between S. mutans and caries has been established in experiments with gnotobiotic rats (Fitzgerald et al., 1960; Gibbons et al., 1966) and conventional hamsters (Keyes, 1960; Fitzgerald and Keyes, 1960). These animals developed caries after exposure to caries-active conspecifics (Keyes, 1960) or after their teeth were inoculated with “caries inducing streptococci” (Fitzgerald and Keyes, 1960) most of which fit the description of S. mutans (Guggenheim, 1968; Edwardsson, 1968). Following these studies, caries was classified as a transmissible infectious disease with S. mutans as the sole pathogen. More recently, other mutans streptococci such as S. sobrinus were classified as similar pathogens by some researchers, although these latter bacteria were less frequently identified in caries lesions, and when present, were in much smaller numbers than S. mutans (Shellis, 2013).
B.Non-specific plaque hypothesis
However, caries has also been found in the absence of S. mutans (van Houte, 1994; Kleinberg, 2002). This finding has led to a shift from the specific plaque hypothesis that necessarily involves pathogenic mutans streptococci such as S. mutans, to the mixed/non-specific plaque hypothesis (Kleinberg, 2002; Kianoush et al., 2014). In this latter hypothesis, a wide range of acidogenic bacteria are proposed to be involved in the development and progression of caries, with the viridans streptococci including S. mutans, S. sobrinus, S. salivarius, S. sanguis, S. mitis believed to be the initial and main pathogens, followed by secondary invaders including Actinomyces, Bacteroides, spirochetes and lactobacilli (Maripandi et al., 2011). Other bacteria including Bifidobacterium, Propionibacterium, Veillonella, Selenomonas and Atopobium (Kianoush et al., 2014), Prevotella and Fusobacterium can also be associated with caries (Maripandi et al. 2011).
Additionally, recent studies have shown that in addition to bacteria, high numbers of Candida albicans fungi (as yeast, filamentous cells or pseudofilaments) can be found in human dental plaque (Barbieri et al, 2007; Maripandi et al., 2011). Although C. albicans is normally a unicellular oral commensal, it can switch to a pathogenic invasive, multiple filamentous form to infect dental tissues. Moreover, C. albicans and S. mutans appear to interact with the presence of C. albicans enhancing the attachment of S. mutans to teeth and vice versa (Metwalli et al., 2013). S. mutans produces lactic acid which stimulates yeast growth and in turn, yeast growth decreases oxygen levels and produces growth factors for Streptococci. The most common form in which C. albicans occurs with S. mutans is the yeast form with production of blastospores (Barbieri et al., 2007).
C.Ecological plaque hypothesis
Local ecological conditions are also important in the development of caries, as noted in the ecological plaque hypothesis. In this model, a biofilm is considered to consist of a normal resident bacterial community, i.e. a state of eubiosis, whereas caries reflects the presence of an abnormal oral bacterial community, i.e. a dysbiosis (Kidd, 2005). A change in the local environment can result in an imbalance of plaque microflora causing dental demineralisation (Kidd, 2005). Frequent access to dietary fermentable carbohydrates or a decreased clearance of carbohydrates by saliva, e.g. due to a lower saliva secretion rate, can lead to more acid being produced with subsequent demineralisation of tooth substance (Kidd, 2005; Olsen, 2006). A low pH is also beneficial for the growth of acidogenic and aciduric bacteria, thus enhancing the acidifying effect and predisposing the associated dental site to caries.
D.Substantial core model
The substantial core model was proposed after the finding that in a pH range of 4.5-7.8, approximately 60% of the bacteria taxa associated with dental caries (including Leptotrichia and Prevotella species and Streptococcus salivarius) can be found in carious dentine lesions regardless of the pH (Kianoush et. al., 2014). A low diversity in microbiota was present in acidic conditions, whereas the microbial populations were more variable in pH neutral environments.
Little is known about the bacteria that are involved in equine dental caries, although a recent conventional and molecular bacteriological study revealed the presence of a newly discovered bacterial species, i.e. Streptococcus devriesei in cheek teeth infundibular caries lesions (Lundström et al, 2007). Baker (1979) reported that the healthy equine oral cavity often had high numbers of streptococci and micrococci, with low numbers of Lactobacillus spp., Fusobacterium spp. and coliforms and intermediate numbers of anaerobes, Veilonella spp. and hydrogen sulphide producing bacteria. In equine periodontal disease a shift in cultivable bacteria occurred with progression of the disease, with a decrease in gram-positive cocci and rods and an increase in gram-negative aerobes, anaerobes and spirochetes (Baker, 1979).
Equine cheek teeth infundibular caries
Different studies have described very diverse prevalences of equine (maxillary cheek tooth) infundibular caries, varying from 8% (Fitzgibbon et al., 2010) to 100% (Honma et al., 1962). This difference could possibly be explained by cemental hypoplasia being classified as infundibular caries by some authors, and also to age-related differences, as the high prevalence found by Honma et al. (1962) was in horses over 12 years of age.
Using light microscopy and ultrastructural examinations, Kilic et al. (1997) found infundibular caries in 24% (5/21) of maxillary cheek teeth: involving the centre of infundibular cementum in 4 of these teeth and its periphery in one. Most (63%; 10/16) other maxillary cheek teeth contained 1 or 2 small central infundibular channels (termed vascular channels) filled with shrunken connective tissue. In recently erupted teeth, many lateral branches of the central vascular channels extended into the infundibular cementum, reducing in size towards its periphery before terminating adjacent to the cemento-enamel junction.
The presence of areas of cemental hypoplasia in the vascular channels seems to predispose to the development of localised central infundibular caries. It has also been proposed that when areas of hypoplastic infundibular cement are exposed to the oral cavity with dental wear, food and oral micro-organisms enter these defects and predispose to the development of more severe infundibular caries (Baker, 1974; Kilic et al., 1997). This is supported by the finding that the maxillary 09s are usually most severely affected by infundibular cemental hypoplasia and also with infundibular caries (Windley et al., 2009; Fitzgibbon et al., 2010). However a recent clinical survey in donkeys found the 06s to be most commonly affected by infundibular caries (Rodrigues et al., 2013). Infundibular caries may lead to apical infection if caries proceeds through infundibular enamel and the adjacent dentine and pulp become affected (Dacre et al., 2008), or to a pathological dental fracture (most often sagittal – termed caries-related infundibular fractures (Dixon et al. 2014 ) as a result of mechanical weakening of the tooth in advanced caries (Dixon, 2002; Dacre et al., 2007).
The system that is most commonly used for grading equine infundibular (Fig 3) and peripheral caries (Fig 4) is the modification of the Honma (1962) system described by Dacre (2005).