Caries in Prehistoric Man

Dental caries is probably a disease of modern civilization. Anthropologic studies of von Lenhossek revealed that the dolichocephalic skulls of men from preneolithic periods (12,000 BC) did not exhibit dental caries, but brachycephalic skulls of the neolithic period (12,000–3000 BC) contained carious teeth. Apparently the carious lesions were found at or just below the contact areas and an increased frequency of caries at the cementoenamel junction was noted.

Caries Incidence in Modern Societies

By about the 17th century, there was a significant increase in the total caries experience and a smaller increase in the number of carious lesions involving the interproximal contact areas of teeth, characteristic of the pattern and occurrence of caries in modern population.

Extensive studies on the incidence of dental caries from various geographic areas have illustrated the apparent influence of civilization on dental disease. Mellanby in 1934 reviewed the literature on caries in existing primitive races and noted that the incidence was invariably less than that in modern man suggesting isolated populations that have not acquired the dietary habits of modern, industrialized man retain a relative freedom from dental caries. Native population living in the North West territories of Canada, Alaska and Greenland who consumed native food, had a lower evidence of carious lesion (0.1%) compared to those living at trading posts (13%). A comparable effect of diet upon caries was demonstrated by Mellanby in studies on natives of Southern Rhodesia. The determinants of the carious process are essentially local and limited to the oral cavity. Although there may be a certain degree of racial resistance to dental caries, dietary factor appears to be more significant, especially since caries incidence is increased by contact with ‘civilized’ food.

Comprehensive Assessment of Dental Caries Prevalence in Modern-day Population

While dental caries is all pervading in highly industrialized societies, the caries experience varies greatly among countries and even within a country. The difference in caries rates noted in different parts of the world are extreme from rates fewer than one decayed, missing and filled (DMF) tooth per person at all ages up to 39 years in Ethiopia (Littleton, 1963) to 60 times greater in Alaska-Aleuts (Russel et al, 1961). Findings from the Interdepartmental Committee on Nutrition for National Defence (ICNND) and WHO studies (Barmes, 1981) indicate that caries prevalence follows definite regional patterns. It is generally lowest (0.5–1.7 DMF) in Asian and African countries and highest (12–18 DMF) in America and other Western countries. Consistently, low to moderate caries rates were found in populations of the Indo-Chinese peninsula, Malaysia, central and southern Thailand, Burma, South Vietnam, mainland China, Taiwan, India and New Guinea.

Generally, highly industrialized countries have the highest caries indices with decayed, missing, and filled teeth (DMFT) of approximately 4.5. However, within this large group of countries a very high caries pattern of over 5.6 DMFT occurs in New Zealand, Australia, Brazil, and Argentina.

Factors Affecting Caries Prevalence

Current Trends in Caries Incidence

Significant data have been presented since the National Caries Program, USA in 1979–80 to substantiate numerous observations that there has been marked improvement in dental health as measured by prevalence of dental caries, especially in children and young adults, throughout the ‘civilized Western world’. Especially impressive was the increase in the percentage of children classified as caries-free in their permanent dentition. These changes had occurred in the absence of both fluoridation and organized preventive programs. This decrease in caries prevalence is also seen in England, Denmark, Ireland, the Netherlands, New Zealand, Norway, Scotland, and Sweden. A substantial decrease in the prevalence of dental caries has been reported from less developed countries. The cause for this widespread decline in the prevalence of dental caries is multifactorial. In some instances, communal water fluoridation has been present in the areas studied and in other cases organized preventive dentistry programs were available.

However, the time period involved in most of these studies coincides with the introduction and increased utilization of fluoride dentifrices and dietary fluoride supplements, as well as an increased awareness of the importance of oral health. The very limited studies available give no evidence that there is any change; for example, in the pervasiveness of Streptococcus mutans or any changes in dominant serotypes. Emphasis on improved physical health through food, exercise, and decreased carbohydrate consumption all may be the factors that have led to this decline.

Role of Carbohydrates

Reference has been made previously to the finding that members of isolated primitive societies who had a relatively low caries index manifested a remarkable increase in caries incidence after exposure to refined diets. The presence of readily fermentable carbohydrates has been thought to be responsible for their loss of caries resistance.

The early studies of Miller showed that when teeth were incubated in mixtures of saliva and bread or sugar, decalcification occurred. There was no effect on the teeth when meat or fat was used in place of the carbohydrate. Both cane sugar and cooked starches produced acid, but little acid was formed when raw starches were substituted. Volker and Pinkerton reported the production of similar quantities of acid from mixtures of either sucrose or starch incubated with saliva with no difference in acid production between raw and refined sugarcane. The etiology of dental caries involves interplay between oral bacteria, local carbohydrates and the tooth surface that may be shown as follows: Bacteria + sugars + teeth → organic acids → caries.

The cariogenic carbohydrates are dietary in origin, since uncontaminated human saliva contains only negligible amounts regardless of the blood sugar level. Salivary carbohydrates are bound to proteins and other compounds, and are not readily available for microbial degradation. The cariogenicity of a dietary carbohydrate varies with the frequency of ingestion, physical form, chemical composition, route of administration and presence of other food constituents. Sticky, solid carbohydrates, soft retentive foods those that are cleared slowly, monosaccharides and disaccharides are more caries-producing. Plaque organisms produce little acid from the sugar alcohols, sorbitol, and mannitol. Glucose or sucrose fed entirely by stomach tube or intravenously, does not contribute to decay as they are unavailable for microbial breakdown. Meals high in fat, protein or salt reduce the oral retentiveness of carbohydrates.

Role of Microorganisms

Miller demonstrated the presence of microorganisms within the tubules of decayed teeth. These were mainly cocci and leptothrix, as he called them, and laid the foundation for the role of acids elaborated by bacteria in caries production. In 1900, Goadby isolated a gram-positive bacillus from carious dentin and termed it B. necrodentalis. These, he concluded, played a role in decalcification of both enamel and dentin. Later he changed his views, stating that certain streptococci were the active cause of caries. Later in 1922, McIntosh, James and Lazarus-Barlow were concerned with microorganisms capable of lowering the pH to the degree that the enamel was softened. From carious dentin they isolated bacteria which they called Bacillus acidophilus odontolyticus. Around the same time, Clarke in Great Britain isolated a streptococcus from teeth that was found to be in the early stages of the disease. In 1924, he described a new streptococcus species, S. mutans, which was almost always isolated from carious lesions in the teeth of British patients. Although the work was confirmed three years later by McLean, scientific interest in S. mutans lay dormant until its rediscovery in the mid 1960s.

Many of the earlier workers focused attention on L. acidophilus because it was found with such frequency in caries-susceptible persons that it came to be regarded as of etiologic importance. In 1925, Bunting and Palmerlee reported the bacillary forms in every initial lesion of caries similar to those described by McIntosh and they termed them B. acidophilus. Bunting stated in 1928, so definite is this correlation between B. acidophilus and dental caries that, in the opinion of this group, the presence or absence of B. acidophilus in the mouth constitutes a definite criterion of the activity of dental caries that is more accurate than any clinical estimation could be. Furthermore, it was noted that there was a spontaneous cessation of caries coincident with the disappearance of B. acidophilus from the mouth, either from prophylactic, therapeutic or dietetic control.

Bunting, Nickerson and Hard carried out extensive studies on B. acidophilus and reported that it was almost universally absent in the mouths of caries-immune persons, but was usually present in the mouths of caries-susceptible persons. Similar findings were reported in 1927 by Jay and Voorhees, who also found that the presence of L. acidophilus in persons without active caries was often a presage of the development of cavities some months later. Jay reported the isolation of 12 strains of Leptothrix in 1927, but doubted their importance in the carious process even though they produced acid from carbohydrates.

Between this period and the 1940s, numerous studies were carried out in attempts to confirm or deny the existence of a microorganism responsible for dental caries. Harrison observed streptococci to predominate on the surfaces of non-carious rat molars, about half of the strains being acidogenic. On the other hand, in rats with carious lesions, the surface flora consisted primarily of lactobacilli. Microorganisms isolated from the deeper carious cavities were mainly acidogenic streptococci and he thus concluded that there was an apparent relationship of lactobacilli with initial caries and of streptococci with more advanced lesions of dentin. Florestano, in 1942, cultured organisms from the saliva of carious and noncarious persons and studied their acidogenic potential. Aciduric streptococci and staphylococci were isolated from both the groups. Their acid production and presence in large numbers suggested a role in dental caries equal to that of lactobacilli. Bacteriologic studies in recent years have helped clarify the role of various organisms in the etiology of dental caries. Considerable emphasis has been placed on the various diet-bacterial interactions, which are involved in lesion development on different tooth surfaces. Specific microorganisms as well as combinations of microorganisms, including Lactobacillus, S. mutans, Actinomyces species and others, have been studied. Although there may be disagreement as to specifics, there is little doubt that bacteria are indispensable to the production of caries. One or more organisms are implicated in the initiation of caries, while other distinctly different organisms may influence the progression of the disease. Also, there is good evidence that different diet–bacterial interactions are involved in root surface and coronal caries, and they may represent two different diseases from the ecological and microbiological point of view.

In 1960, Keyes demonstrated that under certain laboratory conditions, dental caries in hamsters and rats could be considered an infectious and transmissible disease and therefore subject to those biologic principles which govern any infectious process. Fitzgerald and Keyes showed that even in a so-called caries-inactive strain of hamster, oral inoculation of certain pure cultures of streptococci isolated from hamster caries would induce the typical picture of active dental caries. The caries-inactive strain of hamster was found to have a noncariogenic microflora. These findings have led to interesting speculation about the importance of streptococci in the etiology of dental caries.

Microbial Flora and Dental Caries

It is uniformly agreed that caries cannot occur without microorganisms. Several organisms have been found capable of inducing carious lesions when used as monocontaminants in gnotobiotic (germ-free) rats. These include the mutans group of streptococci, a Streptococcus salivarius strain, Streptococcus mitior, Streptococcus milleri, Streptococcus oralis, Streptococcus sanguis (different strains), Peptostreptococcus intermedius, Lactobacillus acidophilus, Lactobacillus casei, Actinomyces viscosus and Actinomyces naeslundii. In addition, in the same animal system, some streptococcis and lactobacilli such as Lactobacillus fermentum and Streptococcus lactis, were not able to induce caries, suggesting that not all organisms are cariogenic, at the same time caries will not occur even in the complete absence of microorganisms. Different organisms display certain selectivity for the tooth surface they localize and attack (Table 9-1).

A wide variety of organisms are able to initiate pit and fissure caries as they colonize in these retentive areas. A limited number of organisms have proved to colonize smooth surfaces and S. mutans is very significant in this respect. Some of the organisms involved in root caries are different from those in other smooth surface lesions because the initial lesion involves the cementum or dentin and not enamel. Bacteriological sampling of plaque covering caries of the root surfaces has yielded predominantly Actinomyces viscosus. However, other studies have found no difference in the prevalence of A. viscosus on carious versus intact root surface. Strains of Nocardia and S. sanguis, besides causing enamel caries may, at times, also cause root caries. While in the deep dentinal caries, the predominant organism is Lactobacillus, the exact extent to which these organisms participate in human disease is yet to be explored.

Studies in humans are largely based on the mathematical relationship between various streptococci, lactobacilli and dental caries. Available data strongly suggest an active involvement of S. mutans in caries initiation. Strains of S. mutans isolated from humans have proved to be cariogenic in animal studies and S. mutans can almost always be found in plaques over incipient lesions involving pits and fissures or smooth tooth surfaces. Not all studies support a unique or sole relationship between S. mutans and the initiation of caries in humans. The characteristics and properties of some known potentially cariogenic plaque microorganisms are discussed.

Role of Acids

The exact mechanism of carbohydrate degradation to form acids in the oral cavity by bacterial action is not known. It probably occurs through enzymatic breakdown of the sugar, and the acids formed are chiefly lactic acid, although others such as butyric acid are also formed. Since acid production is dependent upon a series of enzyme systems, methods of decreasing this acid formation by interference with certain enzymes could be an effective strategy to decrease caries.

The presence of acids in the oral cavity is of less significance than the localization of acids upon the tooth surface. This suggests a mechanism for holding acids, at a given point, for relatively long periods. Dental plaque fulfils this function. Acid production from carbohydrates have been extensively studied in human plaque. Generally, monosaccharides and disaccharides result in the greatest fall in plaque pH. On the other hand, acid formation is slower upon application of cooked starch. This is possibly because of the slower diffusion of larger starch molecules and acid production that occurs from the comparatively low concentration of maltose released from starch. Fermentation or glycolysis are ways of anaerobic catabolism of carbohydrates, which predominates in plaque and leads to acid production. The end products of glycolysis have the same empirical formulas as the starting substrate in that one molecule of glucose breaks into two molecules of lactic acid.

Organisms such as streptococci and lactobacilli ferment sugars, which produce 90% or more lactic acid as the end product; such bacteria are called homofermentative. Heterofermentatives produce a mixture of metabolites including other organic acids such as propionic, butyric, succinic, and ethanol using divergent metabolic pathways. For example, pyruvic acid, an intermediate metabolite in glycolysis, may be rendered to lactic acid by the enzyme lactic acid dehydrogenase or split into formic acid and acetyl coA by the enzyme pyruvate formate lyase. The acetyl coA is then converted into acetate and ethanol. The proportion of lactic acid or other organic acids formed by plaque may be markedly affected by growth conditions and by the bacterial types present. For example acid accumulation by S. mutans is substantially greater than by S. sanguis or S. mitis and Actinomyces are homolactic in anaerobic conditions but in the presence of carbon dioxide the fermentation is heterolactic with formate, acetate, lactate and succinate as their products.

Role of the Dental Plaque

Dental plaque (microbial plaque or bacterial plaque) is a structure of vital significance demonstrated for the first time in histologic preparations by Williams in 1897. It has been recognized for many years as a contributory factor to at least the initiation of the carious lesion.

Although Miller emphasized the role of foods and the acids produced by their bacterial degradation, he thought that the plaque protected enamel against attack by a carious process. In contrast, GV Black in 1899 regarded plaque to be important in the caries process and described it as “The gelatinous plaque of the caries fungus is a thin, transparent film that usually escapes observation, and which is revealed only by careful search. Neither it is the thick mass of material alba so frequently found upon the teeth, nor is the whitish gummy material known as sordes, which is often prominent in fevers and often present in the mouth in smaller quantities in the absence of fever.”

Plaque is the soft, nonmineralized, bacterial deposit which forms on teeth and dental prostheses that are not adequately cleaned. It characteristically forms on tooth surfaces which are not constantly cleansed, and appears as a tenacious, thin film, which may accumulate to a perceptible degree in 24–48 hours. A characteristic of plaque is that it resists removal by physiologic and oral cleansing forces such as saliva and tongue movement but is removable by toothbrushing. An important component of the dental plaque is acquired pellicle, which forms just prior to or concomitantly with bacterial colonization and may facilitate plaque formation. The pellicle is a glycoprotein that is derived from the saliva and is adsorbed on tooth surfaces. It is not dependent on bacteria but may serve as a nutrient for plaque microorganisms.

Dental plaque, or microcosm, as denoted by Arnim, is variable in both chemical and physical composition. It consists of salivary components such as mucin, desquamated epithelial cells and microorganisms. Plaque is composed of about 80% water and 20% solids. These are rich in bacteria with studies showing approximately 2×10¹¹ bacteria per gram. Bacterial and salivary proteins comprise about one half of the dry weight of plaque. Plaque also contains carbohydrates and lipids, which account for approximately 25% of the plaque’s dry weight. Most of the carbohydrates in the matrix consist of polymers, glucans, fructans, and heterosaccharides synthesized by the bacteria. Some of these polymers are thought to play a role in bacterial attachment and cohesion, and others are more important as a reservoir of fermentable substrates metabolized by bacteria when other more readily utilized carbohydrates in plaque become depleted.

Inorganic components of plaque account for approximately 5–10% of the dry weight of plaque. The concentration of calcium and phosphate in dental plaque is several magnitudes higher than in saliva. This is thought to be due, in part, to the infiltration of salivary proteins containing these constituents in the bound form. These probably include statherin, the salivary protein which, by adsorbing onto early crystal nuclei and preventing crystal growth, maintains super saturation of the fluid phase of plaque with apatite. In addition, bacteria may accumulate polyphosphates, which bind to calcium. Most of the calcium found in plaque is non-ionic and solubilisation occurs as pH drops. Dental calculus (q.v.) is plaque in which mineralization has involved both the plaque matrix and the microorganisms. However, the free surface of calculus usually harbors living bacteria.

There is a general agreement that enamel caries begins beneath the dental plaque. The presence of a plaque; however, does not necessarily mean that a carious lesion will develop at that point. Variations in caries formation have been attributed to the nature of the plaque itself, to the saliva or to the tooth. Extensive study of the bacterial flora of the dental plaque has indicated a heterogeneous nature of the structure. Most workers have stressed the presence of filamentous microorganisms, which grow in long interlacing threads and have the property of adhering to smooth enamel surfaces. Smaller bacilli and cocci then become entrapped in this reticular meshwork. Aciduric and acidogenic streptococci and lactobacilli are particularly numerous in this setup. Occasionally, strains of the filamentous organisms are actively acidogenic through carbohydrate fermentation, but this does not appear to be a general feature of this group.

Bibby (1940) studied the characteristics of different strains of filamentous organisms isolated from dental plaques and noted their ability to adhere to smooth surfaces. Blayney and his associates (1942) pointed out that the time required for the development of definite cavitation representing early caries in an intact enamel surface was several months. Hemmens and his coworkers (1946) believed that dental plaque was the most likely starting point for investigations aimed at understanding the earliest stage of enamel caries. They examined numerous plaques from areas of children’s teeth which became carious during the course of investigation. Aciduric streptococci were the organisms most commonly isolated from plaques during the period of caries activity, being present in varying numbers in 86% of the plaques. α-streptococci were isolated from slightly over 50% of the plaques from carious surfaces and from 75% of those from noncarious surfaces. The greatest incidence of occurrence of lactobacilli in plaque was 57%, but these organisms increased in incidence during that period in which the carious lesions were developing.

Most investigations of the microbiology of the dental plaque have concluded that three basic groups of microorganisms predominate: streptococci, actinomyces and veillonellae. The major strains of streptococci present in plaque are S.mutans, S. sanguis, S. mitior, S. milleri and S. salivarius (uncommonly). Major actinomyces strains include A. viscosus, A. naeslundii, A. israelii, and Rothia dentocariosa. The veillonellae group are the anaerobic gram-negative cocci organisms, chiefly V. parvula and V. alcalescens. Of all these, Streptococcus mutans is considered to be the chief etiologic agent in human dental caries today.

Plaques are classified as supra or subgingival, according to the anatomical area in which they form. Supragingival plaques play an essential role in the pathogenesis of dental caries while marginal and subgingival plaques are responsible for the initiation of periodontal diseases.The amount of plaque can be assessed directly by clinical examination (Fig. 9-2). Often dye solutions, referred to as disclosing agents, are used to stain plaques for visual scoring. Although carious lesions will not develop without plaque, it should be emphasized that plaques can often be relatively innocuous, have buffering capacity and protecting the teeth from exposure to acids present in many foods. However, when plaques contain appreciable proportions of highly acidogenic bacteria such as S. mutans and are exposed to readily fermentable dietary sucrose, they produce sufficient concentrations of acids to demineralise the enamel.