Dental caries is the localized demineralization of the tooth surface caused by organic acid metabolites of oral microorganisms such as Streptococcus mutans. The disease leads to a chronic, progressive destruction of the teeth.
The prevalence of dental caries is most often expressed as dmft (decayed, missing, and filled teeth) for primary dentition and DMFT for permanent teeth (Barmes and Sardo-Infirri, 1977). Internationally, prevalence rates of dmft in 6-year-olds and DMFT in 12-year-olds range from a high of 9.3 per child in Japan and 10.6 per child in Switzerland, respectively, to a low of 0.9 per child in Cameroon and 0.1 in Zambia, respectively. U.S. prevalence rates are intermediate; dmft in 6-year-olds is 3.4 per child and DMFT in 12-year-olds is 4.0 per child (Sreebny, 1982a).
Caries prevalence in the United States has declined in the past 30 years. During 1971-1974, children from 5 to 17 years of age had decay or fillings in an average of 7.06 teeth. By 1981 this number had dropped to 4.77, a 32% decrease (NIDR, 1981). Caries of the tooth crown is still predominantly a disease of children and adolescents, although caries of the root surface of the teeth, secondary to exposure of the root by recession of the gingivae, is becoming more prevalent among older adults (Miller et al., 1987). Less is known about the causes of root caries than about caries of the tooth crown, but possible risk factors include increased longevity of the population and longer retention of teeth in adults (Carlos, 1984).
Although declining in prevalence, dental caries in the United States remains a significant health problem. Rates are highest in the Northeast, lowest in the Southwest, and at intermediate levels elsewhere (NIDR, 1981). Prevalence rates are highest in females of every age group (NIDR, 1981) and in people of both sexes in the lower socioeconomic groups (Ismail et al., 1987). The estimated costs of dental care in the United States amounted to $25.1 billion in 1984, or 6.5% of total health care costs (Levit et al., 1985). In 1990, the costs are projected to be as high as $42 billion (Arnett et al., 1986).
Evidence Associating Dietary Factors with Dental Caries
The relationship of diet to dental caries risk was suspected as early as the fourth century B.C., when Aristotle hypothesized that dental caries was caused by consumption of sweet figs, which stuck to the tooth (Forster, 1927). Current evidence from studies in humans and animals indeed indicates that dental caries does not develop in the absence of fermentable carbohydrates in the diet (Brown, 1975). Evidence also suggests that the cariogenic effect of fermentable carbohydrates can be amplified or attenuated by other dietary factors
as well as by oral microflora and host factors (e.g., genetic susceptibility and the composition and flow of saliva). However, as McDonald (1985a) points out, even after 23 centuries we know only a little more than Aristotle about the relative cariogenicity of foods.
Epidemiologic and Clinical Studies
Among the major carbohydrates in the dietcomplex carbohydrates (e.g., starches) and simple sugars (e.g., sucrose and lactose)sucrose appears to have the greatest cariogenic potential. Using data collected by the World Health Organization, Sreebny (1982a) reported a correlation coefficient of .72 between sugar availability in grams per person per day and DMFT in 12-year-old children in 47 countries. However, the correlation coefficient for dmft in 6-year-old children in 23 countries was only .31. Takeuchi (1961) provided time-trend data supportive of Sreebny's cross-sectional findings and reported that the prevalence of dental caries in Japanese children decreased precipitously during the late 1940s in association with the severe reduction in sugar supplies during World War II. Similar observations were made in Europe (Sognnaes, 1948; Toverud, 1957). In the United States, correlation analyses of time-trend data on per-capita sugar consumption and caries incidence suggest (1) that caries incidence increases when per-capita sugar consumption exceeds 40 g/day in the absence of fluoride use and 50 g/day when fluoride is used and (2) that the increase in caries incidence reaches a plateau when the per-capita consumption reaches approximately 130 g/day (Lehner, 1980; Newbrun, 1982; Sheiham, 1983, 1984; Sreebny, 1982b). As Glinsmann et al. (1986) noted, these data suggest that the current mean intake of added and total sugars in the United States (53 and 95 g/day, respectively) contributes substantially to overall caries risk and that reduction in sugar intake could be expected to reduce that risk. However, findings of other studies indicate that the correlation between sugar intake and caries occurrence is not entirely consistent. For example, caries incidence in Great Britain did not change appreciably from 1940 to 1977, despite an apparent doubling of sugar intake (Jackson, 1979). Likewise, the 32% decline in caries prevalence in the United States in the 1970s appears to have occurred despite a continued high intake of sugars. A similar observation was made in a study by DePaola et al. (1982), who noted that caries incidence in Massachusetts schoolchildren dropped markedly during a period in which total sugar consumption increased and then leveled out. Although total sugar consumption increased during the study period, however, the amount of sucrose consumed actually decreased.
Sucrose in solution stimulates the formation of plaque (Geddes et al., 1978)a substance comprising microbial colonies embedded in a matrix of salivary proteins and extracellular polymers, which may serve as a medium for growth of caries-promoting bacteria. It also increases the mineral content of plaque and saliva, suggesting increased mineral resorption from the teeth (Tenovuo et al., 1984). Frequent rinsing with a sucrose solution over 2 months produced changes characteristic of early demineralization of tooth surfaces (Geddes et al., 1978). Small slabs of bovine enamel attached to human teeth for short periods also underwent demineralization when frequently exposed to sucrose (Pearce and Gallagher, 1979; Tehrani et al., 1983).
Sucrose in foods is also cariogenic. In a clinical trial at the University of Turku in Finland (Scheinin et al., 1975a,b), three groups consuming diets containing sucrose, fructose, and xylitol, respectively, were followed for 2 years. By the study's end, the average number of decayed, missing, or filled tooth surfaces (DMFS) was twice as high in the group consuming sucrose than in the fructose group. The xylitol group had virtually no DMFS. The lower cariogenicity of fructose relative to sucrose may explain in part the inability of some studies to demonstrate a cariogenic potential of presweetened foods such as cereals (Finn and Jamison, 1980; Glass and Fleisch, 1974), which differ considerably in their content of specific sugars (Glinsmann et al., 1986). The decline in caries prevalence in the United States since the 1970s, despite a continued high consumption of total sugars, may be partially due to the nation's increasing consumption of corn-derived sweeteners such as fructose and the declining use of sucrose (Glinsmann et al., 1986).
The composition of dietary carbohydrate also appears to influence cariogenicity. Early enamel erosion, a risk factor for caries, was noted in 12 children ages 9 to 15 years who had consumed large quantities of soft drinks (Asher and Read, 1987). The authors concluded that a major contributing factor was the high citric acid content and resulting low pH of the drinks. Consumption of canned pears and apples has also been noted to lower plaque pHa factor believed to promote
tooth demineralization (Shaw, 1987)to a greater degree than sugar alone (Abelson and Pergola, 1984; Imfeld et al., 1978; Jensen and Schachtele, 1983). Likewise, comparisons of snack foods commonly consumed in the United States and in the United Kingdom demonstrate a wide variability in their ability to increase plaque and salivary acidity (Bibby et al., 1986; Edgar et al., 1975). In these studies, the sugar-to-starch ratio of the snack foods appears to be important, since some items low in sugar but high in starch caused a more severe and prolonged increase in plaque and saliva acidity than snacks high in sugar alone (Bibby et al., 1986; Mörmann and Mühlemann, 1981). The degree of plaque and salivary acidification does not necessarily correlate with the amount of enamel destruction that follows or with the extent of subsequent caries (McDonald, 1985a).
The sequence in which carbohydrate-containing foods are eaten also appears to influence cariogenesis. For example, a sharp decrease in the pH of saliva and plaque has been noted after use of a sugar rinse. The pH returns to baseline after approximately 30 minutes. However, when cheese is consumed 5 minutes after a sugar rinse, the sharp increase in acidity is blunted and the pH returns quickly to baseline (Edgar, 1981; Edgar et al., 1982; Schachtele and Jensen, 1983).
The frequency of carbohydrate consumption also appears to influence caries formation. In a classic cohort study conducted in a mental institution in Vipeholm, Sweden, the frequency of dental caries activity in adult patients was monitored over several years while their diet and eating schedule were controlled. Two important findings were noted. First, dental caries appeared to be influenced more by frequency of sucrose intake than by total amount consumed. Second, solid forms of sugar, which are more easily retained in teeth, appear to be more cariogenic than liquid forms of sucrose (Gustafsson et al., 1952).
In general, epidemiologic and clinical findings support the notion that all dietary carbohydrates are cariogenic to some degree and that cariogenesis is influenced not only by the composition of carbohydrate-containing foods but also by the sequence and frequency with which they are consumed. Beyond this, there are two basic reasons why little is known about the cariogenic potential of specific carbohydrate-containing foods: (1) because of cost and ethical considerations, few studies of specific foods and caries in humans have been or will be conducted and (2) findings from such studies are difficult to generalize to noninstitutionalized humans. Furthermore, it is probably not possible to develop a valid cariogenic index for individual foods, since studies of caries incidence comparing groups consuming and not consuming various food items show little effect due to the strong cariogenic challenge from the rest of the diet (McDonald, 1985a).
Certain foods appear to be protective. As noted previously, consumption of cheese blunts the drop in pH characteristically seen after a sugar rinse (Edgar, 1981). Regular milk consumption by 14-year-old Danish schoolchildren was associated with a lower incidence of caries, but regular milk consumption was a marker of a better diet and could also have been an indicator of better preventive dental care (Hölund, 1987). Consumption of salted peanuts and cheddar cheese increases oral alkalinity (Geddes et al., 1977; Imfeld et al., 1978; Jensen and Schachtele, 1983)a factor believed to protect against caries formation. Cocoa also contains substances that inhibit oral acidification (Paolino, 1982). Starchy fibrous foods require increased mastication and may inhibit cariogenesis by stimulating saliva and maintaining neutral plaque pH (Krasse, 1982). Studies suggest that polyols (sugar alcohols, including the 6-carbon sorbitol and 5-carbon xylitol) are noncariogenic and possibly even anticariogenic. Sorbitol-containing chewing gum, unlike sugar-containing gum, does not appear to promote tooth decay in children (Glass, 1983). Also, as noted earlier, the group on the xylitol diet in the University of Turku study had no DMFS. That finding was attributed to the fact that xylitol is not metabolized by oral microbes (Scheinin, 1976; Scheinin et al., 1975a,b). Substitution of xylitol for sucrose in many Finnish food products has been associated with a dramatic decrease in caries incidence over a 2-year period (Scheinin et al., 1975b). Similarly, the use of xylitol-containing chewing gum was associated in one study with low caries incidence, even in subjects who did not otherwise modify their diets. This led the authors to hypothesize that xylitol is actively anticariogenic rather than noncariogenic (Scheinin et al., 1975c).
With the exception of data on fluoride, there are few data relating dietary components to caries risk in humans. Several investigators have found a beneficial effect of supplemental vitamin D in children up to the age of 10 (McDonald, 1985b) and have suggested that the optimal daily intake is approximately 400 IU (Shaw, 1952). However, other studies have produced conflicting findings (Navia, 1970). As a result, the relationship of
vitamin D to caries risk remains unresolved (McDonald, 1985b).
Of all dietary components exhibiting a protective effect against caries, the most effective is fluoride. In the 1930s, large-scale epidemiologic trials conducted in several suburban Chicago communities and later in 21 cities in four states demonstrated a strong inverse association between natural fluoride concentrations in community water supplies and DMFT prevalence in children ages 12 to 14 years (Dean et al., 1941, 1942). In these studies, DMFT prevalence was found to be approximately 60% lower in populations drinking water with natural flouride concentrations of 1 part per million (ppm) during tooth development than in populations consuming little or no fluoride. Once it was determined that the 1 ppm concentration of fluoride in drinking water is both optimal and safe and that the benefit of fluoride ingestion persists into middle age, a decision was made to undertake a large community trial in which water was fluoridated in three communities in North America (Grand Rapids, Michigan; Newburgh, New York; and Brantford, Ontario). A 50 to 60% reduction in caries prevalence was observed in all three communities, and no major adverse effects were noted in residents of any age (McClure, 1970). The findings from these and subsequent large-scale community trials led the American Dental Association and the U.S. Public Health Service in 1950 to endorse widespread fluoridation of the water supply as a preventive measure against dental caries (Schrotenboer, 1981). At present, approximately 130.8 million people in the United States are drinking water from public supplies with either natural fluoride at optimal levels (i.e., 0.7 to 1.2 ppm, depending on ambient temperature) or with fluoride added to meet optimal levels (T. Reeves, Centers for Disease Control, personal communication, 1987).
Ingestion of fluoride at such levels reduces caries risk in people of all ages. For example, consumption of optimally fluoridated water has been associated with an almost 50% reduction in caries incidence in children (Burt et al., 1986; Driscoll et al., 1981) as well as a reduced risk of root caries in adults (Anonymous, 1987; Stamm and Banting, 1980). Consumption of fluoridated water before the emergence of permanent molars appears most effectiveproducing an average risk reduction of 50 to 60%, which continues for the lifetime of the teeth as long as fluoride intake is maintained (Deatherage, 1943). If fluoride intake is discontinued, caries become more prevalent, but not to the degree that would be expected if there had been no previous exposure to fluoride (Lemke et al., 1970; Weatherell et al., 1977).
Although fluoridated water has been shown to be an effective, safe, and low-cost means of reducing caries risk in the general population, more than 45% of the U.S. population continues to drink water with less than optimal levels of fluoride (T. Reeves, Centers for Disease Control, personal communication, 1987). To address this need, the American Dental Association, the American Academy of Pediatrics, and the American Academy of Pediatric Dentistry have issued guidelines on fluoride supplementation for children receiving less than adequate levels of fluoride in their drinking water (see Table 26-1).
The extent of dietary fluoride supplementation in the United States is not known. In a 1982 survey of 4,000 dentists and 2,000 pediatricians, only 60% of the dentists and 70% of the pediatricians who responded reported prescribing dietary fluoride supplements (Gift and Hoerman, 1985). These figures are comparable with those of an earlier survey in which 81% of pediatricians and 63% of family physicians reported prescribing supplements (Margolis et al., 1980). The lower proportion of prescribers among dentists in both surveys may reflect a smaller number of children under age 2 in dentists' practices or a bias resulting from the survey's relatively low response rates, e.g., 75% and 49% among dentists and physicians,
TABLE 26-1 Recommended Daily Fluoride Supplements for Children in Three Age Categories, Based on Fluoride Concentration in the Water Supplya
Supplementation (ppm) Corresponding to Three Levels of Fluoride in the Water Supply (ppm)
Age of Child(years)b
0.3 to 0.7
0 to 2
2 to 3
3 to 13
a Adapted from Levy (1986). Recommended by the Council on Dental Therapeutics of the American Dental Association, by the Committee on Nutrition of the American Academy of Pediatrics, and by the American Academy of Pediatric Dentistry.
b The American Academy of Pediatrics recommends providing tablets from 2 weeks of age through at least 16 years of age.
respectively, in the 1982 survey (Gift and Hoerman, 1985).
The mechanism by which fluoride protects against root and surface caries is not well understood (Brown and König, 1977; Seichter, 1987). Since fluoride is found in enamel as well as in dentin, it is believed to inhibit caries formation primarily by promoting remineralization of early demineralized areas of the tooth (Driscoll, 1985; Silverstone, 1984) and by exerting an antimicrobial effect, thus suppressing cariogenic oral microflora (Shaw, 1987).
Fluoride is absorbed both systemically and topically (Brown et al., 1977; Ericsson, 1977; Weatherell et al., 1977). During tooth development, systemic fluoride appears to be incorporated into the tooth structure (Sognnaes, 1965; Weatherell et al., 1977). After tooth formation, fluoride is incorporated into the surface crystalline structure of the tooth, primarily through topical agents such as fluoridated water and dentifrices (Weatherell et al., 1977).
Overconsumption of fluoride during tooth development can lead to dental fluorosis characterized by mottling of the tooth surfaces. Consumption of water fluoridated at 1 ppm rarely results in clinical fluorosis of either the teeth or skeleton (Carr et al., 1985); however, other fluoride sources can add to overall fluoride load. For example, fluoride in the food chain is believed to contribute on average 0.2 to 0.6 mg of fluoride per person per day. Foods especially rich in fluoride include chicken, seafoods, and brewed tea (tea can contain as much as 1 to 4 mg of fluoride per cup) (Levy, 1986; McClure, 1970; Newbrun, 1975; Richmond, 1985). Fluoride can also be unintentionally ingested from fluoridated dentifrices, which can provide an average daily fluoride intake of as much as 0.3 mg for children under age 5 (Barnhart et al., 1974). Concern has also been expressed about the elevated fluoride levels in some baby formulas and foods (Adair and Wei, 1978; Singer and Ophaug, 1979). Because fluoride levels can vary considerably with the type of formula or food and where it is processed, manufacturers of infant formulas have reduced levels in their products (American Dental Association Council on Dental Therapeutics, 1984).
Overall, however, as noted in a review by Richmond (1985), the amount of fluoride ingested from foods and from the supervised use of fluoridated dentifrices is small, and when combined with levels in optimally fluoridated drinking water, is well within the margin of safety defined by the American Dental Association Council on Dental Therapeutics (1984). The large data base on fluoride indicates that consumption of optimal levels of fluoride substantially reduces caries incidence with little risk of side effects (e.g., dental fluorosis) and that the growing availability of fluoridated water is probably responsible for much of the decline in caries incidence in the United States over the past 15 to 20 years (Dunning, 1979).
Results of animal studies on dietary carbohydrate and cariogenesis are consistent with those of studies in humans. In rats, for example, the incidence of caries increases with increases in the amounts of sucrose added to the diet; a cariogenic effect is seen at levels as low as 0.1% by weight of diet (Michalek et al., 1977). An increase in caries incidence with increasing sucrose dose has been observed at levels ranging from 8% (Kreitzman and Klein, 1976) to 40% of dietary sucrose (Hefti and Schmid, 1979). The cariogenic potential of sucrose is greater than that of equivalent amounts of glucose, fructose, or invert sugars (a mixture of dextrose and fructose obtained by hydrolyzing sucrose) (Birkhed et al., 1981; Horton et al., 1985).
As in humans, the cariogenicity of dietary carbohydrates in animal models appears to be influenced by the frequency, form, and composition of the diet. For example, frequent consumption of carbohydrates markedly accelerates caries formation in rats (Firestone et al., 1982; Skinner et al., 1982). Studies of the cariogenic potential of various forms of dietary carbohydrates in rats indicate that certain carbohydrate-containing foods, such as bananas, are much more cariogenic than sucrose alone or even sucrose-topped chocolate fed frequently in meals (Shrestha and Kreutler, 1983). Consumption of a cereal base with added sugar caused fewer caries in rats than did consumption of presweetened cereals with equal sucrose levels (McDonald and Stookey, 1977). Likewise, carbohydrates in the form of maize or wheat starch had virtually no cariogenic activity when consumed by gnotobiotic rats and macaques, respectively (Beighton and Hayday, 1984; Horton et al., 1985).
Studies of dietary composition in rats indicate that addition of certain cheeses (e.g., cheddar cheese) to a cariogenic diet protects against buccal (cheek side) decay both alone (Edgar et al., 1982; Harper et al., 1986) and with sulcal caries (toward the linear depression in the occlusal surface of the
tooth) (Rosen et al., 1984). Other dietary substances inhibiting sucrose cariogenicity in animal models include mineral concentrates containing protein, calcium, and phosphate (Harper et al., 1987); cocoa (Paolino, 1982); and xylitol (Leach and Green, 1981; Shyu and Hsu, 1980) in rats; and saccharin in inbred hamsters (Linke, 1980). The mechanisms by which these items inhibit sucrose cariogenicity in animal models are not clearly understood, but may include enzyme inhibition in oral bacteria (Paolino, 1982); stimulation of saliva, which helps to maintain plaque pH in a neutral range (Krasse, 1982); and the influence of the texture and casein or calcium-phosphate content of cheeses (Harper et al., 1986).
The cariogenicity of other dietary components, including protein, vitamin D, niacin, pyridoxine, calcium, phosphorus, and certain trace elements, has also been investigated in animal studies. Offspring of rats fed marginal protein diets during pregnancy and lactation developed molars that were much more prone to caries than offspring of rats fed adequate protein diets (Shaw and Griffiths, 1963). Shaw (1987) hypothesized that the decreased amount and altered protein content of saliva in the protein-depleted rats may account for part of their increased caries susceptibility. Other studies have shown that children with protein-calorie malnutrition have not only a high rate of caries but also reduced salivary levels of immunoglobulin A (IgA), the predominant immunoglobulin in body secretions (McMurray et al., 1977; Reddy et al., 1976). McDonald (1985b) hypothesized that protein malnutrition disturbs IgA salivary concentration, thereby increasing caries risk.
In one early study in puppies, vitamin D deficiency was shown to disturb the rate of tooth eruption, tooth position, and calcification of enamel on permanent teeth (Mellanby, 1918). The B-complex vitamins niacin and pyridoxine were also shown in early studies to modify cariogenesis in animals; however, unlike vitamin D, their effect did not appear to be systemic. Niacin was believed to promote caries formation in the Syrian hamster by stimulating oral microflora (Orland et al., 1950). Unlike niacin, pyridoxine seemed to suppress caries formation in animals (Strean et al., 1956) and in humans (Strean, 1958). The paucity of more recent evidence on these vitamins suggests that neither plays a major role in cariogenesis.
The roles of calcium and phosphorus, both major constituents of teeth, were also the subject of early research (McDonald, 1985b). Reduction of dietary calcium in rats was shown to increase caries risk (Constant et al., 1954; Gustafson et al., 1963), whereas the addition of calcium chloride, calcium gluconate, or phosphorus decreased risk (Gustafson et al., 1964; Stanmeyer, 1963). There has been no confirmation of these findings, however. A number of trace elements, including aluminum, barium, boron, cadmium, copper, lead, and selenium, have also been examined for cariostatic potential, but again, no definitive data have been obtained (Losee and Ludwig, 1970).
Animal studies support findings in humans that dietary carbohydrates, especially sucrose, are a major risk factor for caries and that the frequency and sequence of carbohydrate consumption as well as the composition of the carbohydrates can also influence cariogenicity. Interpretation of the results from such studies must be tempered, however, by the knowledge that most of them are derived from a single animal speciesthe rat. The rat has been favored because of the rapidity with which it develops dental caries in the laboratory and the similarity of its sulcal and smooth-surface carious lesions to those of humans (Glinsmann et al., 1986); however, its feeding patterns and oral physiology (e.g., microbial composition, oral pH, salivary composition, flow rate, and buffering capacity) differ greatly from those of humans (McDonald, 1985a). For example, rats nibble throughout the day, and it is known that meal frequency correlates positively and strongly with caries formation in animals (Firestone et al., 1982; Skinner et al., 1982) and in humans (Gustafsson et al., 1952). Furthermore, foods must be given to rats in powdered formnot in the physical form usually consumed by humans. This can complicate attempts to assess cariogenicity of specific foods (Krasse, 1985). Differences in oral physiology may also .influence findings. For example, although most types of phosphates effectively reduce caries in rats when added to sucrose-containing diets, phosphate supplementation in the human diet has been markedly unsuccessful in reducing caries incidence (Nizel and Harris, 1964).
Evidence Associating Nondietary Factors with Dental Caries
Studies suggest that fermentable carbohydrates in the diet contribute to caries formation but are not sufficient by themselves to cause dental caries. Oral microflora and appropriate host factors must also be present and must interact with diet if caries are to form and progress (Navia, 1977).
The oral cavity is host to a variety of microbial flora that thrive in the moist nutrient-rich environment. At birth, the mouth is usually sterile; soon afterward, colonization occurs (Gibbons and van Houte, 1978). The cariogenic role of oral microflora was first noted in studies of rats delivered by Caesarean section and maintained under sterile conditions. The germ-free rats were caries-free from birth and remained so, even when fed a cariogenic diet (Orland et al., 1954).
Streptococcus mutans is most commonly associated with cariogenesis. S. mutans has been found in all human populations and is concentrated in plaque over the most active carious lesions (Kristofferson et al., 1985). Bacteriocin typing of S. mutans demonstrates that the mother is the major source of oral infection in the infant (Berkowitz and Jordan, 1975; Rogers, 1981). The mother also determines the extent of infection, since highly infected mothers tend to have children with higher counts of S. mutans than mothers with low infection rates (Köhler and Bratthall, 1978).
Both the presence and the extent of S. mutans infection in children are associated with caries risk. Köhler et al. (1986) reported that in children infected with S. mutans before age 2, caries prevalence is 8 times greater than in children not infected until age 4. Similarly, children who are more heavily infected tend to develop more caries than children with lower counts (Köhler et al., 1984).
Monoinoculation of germ-free rats with various isolates of human oral microflora has demonstrated that most strains of S. mutans can cause caries in the fissures and smooth surfaces of the teeth, although strains vary in virulence. Other microorganisms associated to various degrees with caries formation include Streptococcus salivarius, S. sanguis, Lactobacillus casei, and several strains of Actinomyces (Miller, 1981). However, generalizing these findings to humans should be approached with caution, since monoinfection in gnotobiotic rats does not mimic the process that occurs in the oral environment of humans where various microflora compete for available niches (Shaw, 1987).
The mechanisms by which S. mutans, S. sanguis, and other microorganisms promote caries are not well understood. S. sanguis is believed to help establish colonization of the tooth surface by S. mutans and other oral microflora (van Houte, 1976). If unimpeded, progressive colonization of the tooth surface results in plaque (Hardie and Bowden, 1976). Plaque holds acidic microbial metabolic by-products close to the tooth surface, protecting them from the buffering effect of saliva. These by-products are believed to demineralize the tooth surface and promote decay. The microbial content of plaque can vary considerably, however, both across a single tooth surface and over time. This limits our ability to identify specific causative agents. Furthermore, S. mutans is often not detectable in plaque over apparently active carious lesions (Shaw, 1987). Whether this results from an inability to measure small microbial concentrations, from mistaken sampling of inactive lesions, or from a true lack of effect is not known. However, the association of S. mutans infection with caries incidence in children and the fact that plaque concentrations over active lesions are reduced when sugar consumption is curtailed suggests that S. mutans is a major etiologic agent for caries of the tooth crown.
The role of genetic susceptibility in caries causation appears to be minor. Although monozygotic twins in one longitudinal twin study were found to have a more concordant incidence rate of caries than dizygotic twins (Kent and Moorrees, 1979), corroborative evidence is lacking.
The composition and the rate of flow of saliva appear to influence cariogenesis in several ways, although there is no evidence for genetic determination of these factors (Shaw, 1987). Saliva can act as a buffer, neutralizing acid by-products of oral microflora found on tooth surfaces and in carious lesions. The high concentrations of calcium and phosphorus and the low levels of fluoride found in saliva may facilitate remineralization of early carious lesions and form caries-resistant surface enamel (Silverstone, 1984). Saliva may also inhibit the metabolism and growth of cariogenic microflora, since it contains several potentially bacteriostatic agents, including lysozyme, lactoferrin, and secretory immunoglobulins (Cole et al., 1976; Evans et al., 1976; Pollock et al., 1976).
Decreasing saliva flow in rodents through removal or ligation of some or all the major salivary glands substantially increases caries incidence (Muhler and Shafer, 1957; Schwartz and Shaw, 1955; Schwartz and Weisberger, 1955). Destruction or absence of salivary glands in humans results in a marked increase in caries incidence (Bertram, 1967).
Dental caries is a multifactorial disease. Diet and oral microflora are implicated in caries causation along with such host factors as salivary composition and flow. Genetic susceptibility does not appear to be a major risk factor for caries.
Fermentable carbohydrates appear to be the only component of the diet capable of inducing caries. All fermentable dietary carbohydrates, especially sucrose, are potentially cariogenic, but sucrose is generally accepted as the most cariogenic dietary factor. Sucrose consumption has been associated most strongly by and consistently with the frequency of dental caries in humans. Other sugars such as glucose and fructose have also been shown to be potentially cariogenic in human and laboratory studies, although they appear to be less cariogenic than sucrose. The cariogenic potential of carbohydrate-containing foods depends on their characteristics (e.g., stickiness), and the frequency and sequence of their consumption. The addition of certain foods and nonnutritive sweeteners, such as cheddar cheese, cocoa, and xylitol, to the diet appears to reduce the cariogenic potential of a sucrose-containing meal.
Caries will neither form nor progress in the absence of a suitable substrate (e.g., oral microflora). Of the oral microflora that have been implicated in caries causation, S. mutans has been the most consistently and strongly associated.
Consumption of fluoride in optimal amounts reduces caries incidence in people of all ages. Fluoride is strongly anticariogenic if consumed in optimal amounts before eruption of permanent teeth. Widespread fluoridation of water supplies and the use of topical fluorides (e.g., fluoridated dentifrices), combined with changing trends in sugar consumption (e.g., decreasing sucrose consumption), are probably the two factors most responsible for the recent decline in caries prevalence rates in the United States.
Directions for Research
· Research should be continued on plaque and its specific role in cariogenesis and on dietary factors and food intake patterns that can modify plaque ecology or prevent plaque accumulation.
· More research should be undertaken on the environmental and genetic factors that influence risk of tooth and root cavities.
Abelson, D.C., and G. Pergola. 1984. The effect of sucrose concentration on plaque pH in vivo. Clin. Prevent. Dent. 6:23-26.
Adair, S.M., and S.H.Y. Wei. 1978. Supplemental fluoride recommendations for infants based on dietary fluoride intake. Caries Res. 12:76-82.
American Dental Association Council on Dental Therapeutics. 1984. Fluoride compounds. Pp. 395-420 in Accepted Dental Therapeutics, 40th ed. American Dental Association, Chicago.
Anonymous. 1987. Fluoride and root surface caries. Nutr. Rev. 45:103-105.
Arnett, R.H., III, D.R. McKusick, S.R. Sonnefield, and C.S. Cowell. 1986. Projections of health care spending to 1990. Health Care Finan. Rev. 7:1-36.
Asher, C., and M.J.F. Read. 1987. Early enamel erosion in children associated with the excessive consumption of citric acid. Pediatr. Dent. 162:384-387.
Barmes, D.E., and J. Sardo-Infirri. 1977. World Health Organization activities in oral epidemiology. Community Dent. Oral Epidemiol. 5:22-29.
Barnhart, W.E., LK. Hiller, G.J. Leonard, and E. Michaels. 1974. Dentifrice usage and ingestion among four age groups. J. Dent. Res. 53:1317-1322.
Beighton, D., and H. Hayday. 1984. The establishment of the bacterium Streptococcus mutans in dental plaque and the induction of caries in macaque monkeys (Macaca fascicularis) fed a diet containing cooked wheat flour. Arch. Oral Biol. 29:369-372.
Berkowitz, R.J., and H.V. Jordan. 1975. Similarity of bacteriocins of Streptococcus mutans from mother and infant. Arch. Oral Biol. 20:725-730.
Bertram, U. 1967. Xerostomia. Clinical aspects, pathology and pathogenesis. Acta Odont. Scand. 25 suppl. 49:1-126.
Bibby, B.G., S.A. Mundorff, D.T. Zero, and K.J. Almekinder. 1986. Oral food clearance and the pH of plaque and saliva. J. Am. Dent. Assoc. 112:333-337.
Birkhed, D., V. Topitsoglou, S. Edwardsson, and G. Frostell. 1981. Cariogenicity of invert sugar in long-term rat experiments. Caries Res. 15:302-307.
Brown, A.T. 1975. The role of dietary carbohydrates in plaque formation and oral disease. Nutr. Rev. 33:353-361.
Brown, W.E., and K.G. König, eds. 1977. Cariostatic mechanisms of fluorides. Caries Res. 11 suppl. 1:1-327.
Brown, W.E., T.M. Gregory, and L.C. Chow. 1977. Effects of fluoride on enamel solubility and cariostasis. Caries Res. 11 suppl. 1:118-141.
Burt, B.A., S.A. Eklund, and W.J. Loesche. 1986. Dental benefits of limited exposure to fluoridated water in childhood. J. Dent. Res. 65:1322-1325.
Carlos, J.P. 1984. Epidemiologic trends in caries: impact on adults and the aged. Pp. 131-148 in B. Guggenheim, ed. Cariology Today. S. Karger, Basel.
Carr, L.M., G.G. Craig, R. MacLennan, T.J. Martin, N.H. Stacey, and R. Woods. 1985. Fluorides in the control of dental caries. J. Food Nutr. 42:178-188.
Cole, M.F., R.R. Arnold, J. Mestecky, S. Prince, R. Kulhavy, and J.R. McGhee. 1976. Studies with human lactoferrin and Streptococcus mutans. Pp. 359-373 in H.M. Stiles, W.J. Loesche, and T.C. O'Brien, eds. Microbial Aspects of Dental Caries, Vol. 2. Information Retrieval, Inc., Washington, D.C.
Constant, M.A., H.W. Sievert, P.H. Phillips, and C.A.
Elvehjem. 1954. Dental caries in cotton rat: effect of tooth maturity and minerals on caries production by semi-synthetic diets. J. Nutr. 53:29-41.
Dean, H.T., P. Jay, F.A. Arnold, Jr., and E. Elvove. 1941. Domestic water and dental caries: study of 2,832 white children, aged 12-14 years, of 8 suburban Chicago communities, including Lactobacillus acidophilus studies of 1,761 children. Public Health Rep. 56:761-792.
Dean, H.T., F.A. Arnold, Jr., and E. Elvove. 1942. Domestic water and dental caries: additional studies of relation of fluoride domestic waters to dental caries experience in 4,425 white children aged 12 to 14 years, of 13 cities in 4 states. Public Health Rep. 57:1155-1179.
Deatherage, C.F. 1943. Fluoride domestic waters and dental caries experience in 2,026 white Illinois selective service men. J. Dent. Res. 22:129-137.
DePaola, P.F., P.M. Soparkar, M. Tavares, M. Allukian, Jr., and H. Peterson. 1982. A dental survey of Massachusetts school children. J. Dent. Res. (sp. iss.) 61:1356-1360.
Driscoll, W.S. 1985. What we know and don't know about dietary fluoride supplementsthe research basis. J. Dent. Child. 52:259-264.
Driscoll, W.S., S.B. Heifetz, and J.A. Brunelle. 1981. Caries-preventive effects of fluoride tablets in schoolchildren four years after discontinuation of treatments. J. Am. Dent. Assoc. 103:878-881.
Dunning, J.M. 1979. Water fluoridation. Pp. 377-414 in Principles of Dental Public Health, 3rd ed. Harvard University Press, Cambridge, Mass.
Edgar, W.M. 1981. Effect of sequence in food intake on plaque pH. Pp. 279-287 in J.J. Hefferren and H.M. Koehler, eds. Foods, Nutrition and Dental Health, Vol. 1. Pathotox Publ., Park Forest South, Ill.
Edgar, W.M., B.G. Bibby, S. Mundorff, and . Rowley. 1975. Acid production in plaques after eating snacks: modifying factors in foods. J. Am. Dent. Assoc. 90:148-425.
Edgar, W.M., W.H. Bowen, S. Amsbaugh, E. Monell-Torrens, and J. Brunelle. 1982. Effects of different eating patterns on dental caries in the rat. Caries Res. 16:384-389.
Ericsson, S.Y. 1977. Cariostatic mechanisms of fluorides: clinical observations. Caries Res. II suppl. 1:2-41.
Evans, R.T., R.J. Genco, F.G. Emmings, and R. Linzer. 1976. Antibody in the prevention of adherence: measurement of antibody to purified carbohydrates of Streptococcus mutans with an enzyme linked immunosorbent assay. Pp. 375-386 in H.M. Stiles, W.J. Loesche, and T.C. O'Brien, eds. Microbial Aspects of Dental Caries, Vol. 2. Information Retrieval, Inc., Washington, D.C.
Finn, S.B., and H.C. Jamison. 1980. The relative effects of three dietary supplements on dental caries. J. Dent. Child. 47:109-113.
Firestone, A.R., R. Schmid, and H.R. Mühlemann. 1982. Cariogenic effects of cooked wheat starch alone or with sucrose and frequency controlled feedings in rats. Arch. Oral Biol. 27:759-763.
Forster, E.S. 1927. The works of Aristotle, Vol. VII. Problemata. Oxford University Press, London. 931 pp.
Geddes, D.A., W.M. Edgar, G.N. Jenkins, and A.M. Rugg-Gunn. 1977. Apples, salted peanuts and plaque pH. Br. Dent. J. 142:317-319.
Geddes, D.A., J.A. Cooke, W.M. Edgar, and G.N. Jenkins. 1978. The effect of frequent sucrose mouthrinsing on the induction in vivo of caries-like changes in human dental enamel. Arch. Oral Biol. 23:663-665.
Gibbons, R.J., and J. van Houte. 1978. Oral bacterial ecology. Pp. 684-705 in J.H. Shaw, E.A. Sweeney, C.C. Cappuccino, and S.M. Meller, eds. Textbook of Oral Biology. W.B. Saunders, Philadelphia.
Gift, H.C., and K.C. Hoerman. 1985. Attitudes of dentists and physicians toward the use of dietary fluoride supplements. J. Dent. Child. 52:265-268.
Glass, R.L. 1983. A two-year clinical trial of sorbitol chewing gum. Caries Res. 17:365-368.
Glass, R.L., and S. Fleisch. 1974. Diet and dental caries: dental caries incidence and the consumption of ready-to-eat cereals. J. Am. Dent. Assoc. 88:807-813.
Glinsmann, W.H., H. Irausquin, and Y.K. Park. 1986. Evaluation of health aspects of sugars contained in carbohydrate sweeteners: report of Sugars Task Force, 1986. J. Nutr. 116:S1-S216.
Gustafson, G., E. Stelling, and E. Brunius. 1963. Cariogenic effect of variations in the salt mixture in a synthetic cariogenic diet. Experimental dental caries in golden hamsters, XI. Acta Odont. Scand. 21:297-308.
Gustafson, G., E. Stelling, and E. Brunius. 1964. Dietary calcium and caries. Experimental dental caries in golden hamsters. Acta Odont. Scand. 22:477-485.
Gustafsson, B.E., C.E. Quensel, L.S. Lanke, C. Lundqvist, H. Grahnen, B.E. Bonow, and B. Krasse. 1952. Vipeholm Dental Caries Study: the effect of different levels of carbohydrate intake on caries activity in 436 individuals observed for five years (Sweden). Acta Ondont. Scand. 11:232-364.
Hardie, J.M., and G.H. Bowden. 1976. The microbial flora in dental plaque: bacterial succession and isolation considerations. Pp. 63-86 in H.M. Stiles, W.J. Loesche, and T.C. O'Brien, eds. Microbial Aspects of Dental Caries, Vol. 1. Information Retrieval, Inc., Washington, D.C.
Harper, D.S., J.C. Osborn, J.J. Hefferren, and R. Clayton. 1986. Cariostatic evaluation of cheeses with diverse physical and compositional characteristics. Caries Res. 20:123-130.
Harper, D.S., J.C. Osborn, R. Clayton, and J.J. Hefferren. 1987. Modification of food cariogenicity in rats by mineral-rich concentrates from milk. J. Dent. Res. 66:42-45.
Hefti, A., and R. Schmid. 1979. Effect on caries incidence in rats of increasing dietary sucrose levels. Caries Res. 13:298-300.
Hölund, U. 1987. Relationship between diet-related behavior and caries in a group of 14-year-old Danish children. Community Dent. Oral Epidemiol. 15:184-187.
Horton, W.A., A.E. Jacobs, R.M. Green, V.F. Hillier, and D.B. Drucker. 1985. The cariogenicity of sucrose, glucose and maize starch in gnotobiotic rats mono-infected with strains of the bacteria Streptococcus mutans, Streptococcus salivarius, and Streptococcus milleri. Arch. Oral Biol. 30:777-780.
Imfeld, T., R.S. Hirsch, and H.R. Mühlemann. 1978. Telemetric recordings of interdental plaque pH during different meal patterns. Br. Dent. J. 144:40-45.
Ismail, A.L., B.A. Burt, and J.A. Brunelle. 1987. Prevalence of dental caries and periodontal disease in Mexican American children aged 5 to 17 years: results from southwestern HHANES, 1982-83. Am. J. Public Health 77:967-970.
Jackson, D. 1979. Caries experience in deciduous teeth of five-year-old English children: 1974-1977. Probe 20:404-406.
Jensen, M.E., and C.F. Schachtele. 1983. The acidogenic potential of reference foods and snacks at interproximal sites in the human dentition. J. Dent. Res. 62:889-892.
Kent, R.L., Jr., and C.F.A. Moorrees. 1979. Associations in interproximal caries prevalence from a longitudinal twin study. J. Dent. Res. (sp. iss.) 58:225.
Köhler, B., and D. Bratthall. 1978. Intrafamilial levels of Streptococcus mutans and some aspects of the bacterial transmission. Scand. J. Dent. Res. 86:35-42.
Köhler, B., I. Andréen, and B. Jonsson. 1984. The effect of caries-preventive measures in mothers on dental caries and the oral presence of the bacteria Streptococcus mutans and lactobacilli in their children. Arch. Oral Biol. 29:879-883.
Köhler, B., I. Andreen, and B. Jonsson. 1986. Streptococcus mutans infection and dental caries in young childrena longitudinal study. Caries Res. 20:171.
Krasse, B. 1982. Oral effect of other carbohydrates. Int. Dent. J. 32:24-32.
Krasse, B. 1985. The cariogenic potential of foodsa critical review of current methods. Int. Dent. J. 35:36-42.
Kreitzman, S.N., and R.M. Klein. 1976. Non-linear relationship between dietary sucrose and dental caries. J. Dent. Res. (sp. iss.) 55:B175.
Kristofferson, K., H.G. Grödahl, and D. Bratthall. 1985. The more Streptococcus mutans, the more caries on approximal surfaces. J. Dent. Res. 64:58-61.
Leach, S.A., and R.M. Green. 1981. Reversal of fissure caries in the albino rat by sweetening agents. Caries Res. 15:508-511.
Lehner, T. 1980. Future possibilities for the prevention of caries and periodontal disease. Br. Dent. J. 149:318-325.
Lemke, C.W., J.M. Doherty, and M.C. Arra. 1970. Controlled fluoridation: the dental effects of discontinuation in Antigo, Wisconsin. J. Am. Dent. Assoc. 80:782-786.
Levit, K.R., H. Lazenby, D.R. Waldo, and L.M. Davidoff. 1985. National health expenditures, 1984. Health Care Finan. Rev. 7:1-35.
Levy, S.M. 1986. Expansion of the proper use of systemic fluoride supplements. J. Am. Dent. Assoc. 112:30-34.
Linke, H.A. 1980. Inhibition of dental caries in the inbred hamster by saccharin. Ann. Dent. 39:71-74.
Losee, F.L., and T.G. Ludwig. 1970. Trace elements and caries. J. Dent. Res. 49:1229-1236.
Margolis, F.J., B.A. Burt, M.A. Schork, R.L. Bashshur, B.A. Whittaker, and T.L. Burns. 1980. Fluoride supplements for children: a survey of physicians' prescription practices. Am. J. Dis. Child. 134:865-868.
McClure, F.J. 1970. Water fluoridation: the search and the victory. National Institute of Dental Research, National Institutes of Health, Public Health Service, U.S. Department of Health, Education, and Welfare, Bethesda, Md. 302 pp.
McDonald, J.L., Jr. 1985a. Cariogenicity of foods. Pp. 320-345 in R.L. Pollack and E. Kravitz, eds. Nutrition in Oral Health and Disease. Lea & Febiger, Philadelphia.
McDonald, J.L, Jr. 1985b. Dietary and nutritional influences on caries. Pp. 151-160 in R.L. Pollack and E. Kravitz, eds. Nutrition in Oral Health and Disease. Lea & Febiger, Philadelphia.
McDonald, J.L, Jr., and G.K. Stookey. 1977. Animal studies concerning the cariogenicity of dry breakfast cereals. J. Dent. Res. 56:1001-1006.
McMurray, D.N., H. Rey, L.J. Casazza, and R.R. Watson. 1977. Effect of moderate malnutrition on concentrations of immunoglobulins and enzymes in tears and saliva of young Colombian children. Am. J. Clin. Nutr. 30:1944-1948.
Mellanby, M. 1918. The influence of diet on tooth formation. Lancet 2:767-770.
Michalek, S.M., J.R. McGhee, T. Shiota, and D. Devenyns. 1977. Low sucrose levels promote extensive Streptococcus mutans-induced dental caries. Infect. Immun. 16:712-714.
Miller, A.J., J.A. Brunelle, J.P. Carlos, L.J. Brown, and H. Löe. 1987. Oral Health of United States Adults. The National Survey of Oral Health in U.S. Employed Adults and Seniors: 1985-1986, National Findings. NIH Publ. No. 87-2868. Epidemiology and Oral Disease Prevention, National Institute of Dental Research, National Institutes of Health, Public Health Service, U.S. Department of Health and Human Services, Bethesda, Md. 168 pp.
Miller, C.H. 1981. Dental caries. Pp. 340-363 in G.J. Roth and R. Calmes, eds. Oral Biology. C.V. Mosby, St. Louis.
Mörmann, J.E., and H.R. Mühlemann. 1981. Oral starch degradation and its influence on acid production in human dental plaque. Caries Res. 15:166-175.
Muhler, J.C., and W.G. Shafer. 1957. Comparison between salivary gland extirpation and duct ligation on dental caries in rats. J. Dent. Res. 36:886-888.
Navia, J.M. 1970. Evaluation of nutritional and dietary factors that modify animal caries. J. Dent. Res. 49:1213-1228.
Navia, J.M. 1977. Experimental dental caries. Pp. 257-297 in Animal Models in Dental Research. University of Alabama Press, Tuscaloosa, Ala.
Newbrun, E., ed. 1975. Fluorides and Dental Caries, 2nd ed. C.C. Thomas, Springfield, Ill.. 208 pp.
Newbrun, E. 1982. Sugar and dental caries: a review of human studies. Science 217:418-423.
NIDR (National Institute of Dental Research). 1981. The Prevalence of Dental Caries in United States Children: 1979-1980. NIH Publ. No. 82-2245. National Caries Program, National Institutes of Health, Public Health Service, U.S. Department of Health and Human Services, Bethesda, Md. 159 pp.
Nizel, A.E., and R.S. Harris. 1964. Effects of phosphates on experimental dental caries: a literature review. J. Dent. Res. 43:1123-1136.
Orland, F.J., E.S. Hemmens, and R.W. Harrison. 1950. Effect of partly synthetic diets on the dental caries incidence in Syrian hamsters. J. Dent. Res. 29:512-528.
Orland, F.J., R. Blayney, R.W. Harrison, J.A. Reyniers, P.C. Trexler, M. Wagner, H.A. Gordon, and T.D. Luckey. 1954. Use of the germ-free animal technic in the study of experimental dental caries. I. Basic observations on rats reared free of all microorganisms. J. Dent. Res. 33:147-174.
Paolino, V. 1982. Anti-plaque activity of cocoa. Pp. 43-58 in J.J. Hefferren and H.M. Koehler, eds. Foods, Nutrition and Dental Health, Vol. 2: Third Annual Conference. American Dental Association, Chicago.
Pearce, E.I., and I.H. Gallagher. 1979. The behaviour of sucrose and xylitol in an intro-oral caries test. N.Z Dent. J. 75:8-14.
Pollock, J.J., V.J. Iacono, H.G. Bicker, B.J. MacKay, L.I. Katona, L.B. Taichman, and E. Thomas. 1976. The binding, aggregation and lytic properties of lysozyme. Pp. 325-352 in H.M. Stiles, W.J. Loesche, and T.C. O'Brien, eds. Microbial Aspects of Dental Caries, Vol. 2. Information Retrieval, Inc., Washington, D.C.
Reddy, V., N. Raghuramulu, and C. Bhaskaram. 1976. Secretory IgA in protein-calorie malnutrition. Arch. Dis. Child. 51:871-874.
Richmond, V.L. 1985. Thirty years of fluoridation: a review. Am. J. Clin. Nutr. 41:129-138.
Rogers, A.H. 1981. The source of infection in the intrafamilial transfer of Streptococcus mutans. Caries Res. 15:26-31.
Rosen, S., D.B. Min, D.S. Harper, W.J. Harper, W.X. Beck, and F.M. Beck. 1984. Effect of cheese, with and without sucrose, on dental caries and recovery of Streptococcus mutans in rats. J. Dent. Res. 63:894-896.
Schachtele, C.F., and M.E. Jensen. 1983. Can foods be ranked according to their cariogenic potential? Pp. 136-146 in B. Guggenheim, ed. Cariology Today. S. Karger, Basel.
Scheinin, A. 1976. Caries control through the use of sugar substitutes. Int. Dent. J. 26:4-13.
Scheinin, A., K.K. Mäkinen, and K. Ylitalo. 1975a. Turku sugar studies. I. An intermediate report on the effect of sucrose, fructose and xylitol diets on the caries incidence in man. Acta Ondont. Scand. 32:383-412.
Scheinin, A., K.K. Makinen, and K. Ylitalo. 1975b. Turku sugar studies. V. Final report on the effect of sucrose, fructose and xylitol diets on the caries incidence in man. Acta Odont. Scand. 33:67-104.
Scheinin, A., K.K. Mäkinen, E. Tammisalo, and M. Rekola. 1975c. Turku sugar studies. XVIII. Incidence of dental caries in relation to 1-year consumption of xylitol chewing gum. Acta Odont. Scand. 33:307-316.
Schrotenboer, G.H. 1981. Fluoride benefitsafter 36 years. J. Am. Dent. Assoc. 102:473-474.
Schwartz, A., and J.H. Shaw. 1955. Studies on the effect of selective desalivation on the dental caries incidence of albino rats. J. Dent. Res. 34:239-247.
Schwartz, A., and D. Weisberger. 1955. Salivary factors in experimental animal caries. Pp. 125-136 in R.F. Sognnaes, ed. Advances in Experimental Caries Research. American Association for the Advancement of Science, Washington, D.C.
Seichter, U. 1987. Root surface caries: a critical literature review. J. Am. Dent. Assoc. 115:305-310.
Shaw, J.H. 1952. Nutrition and dental caries. Pp. 415-507 in G. Toverud, S.B. Finn, G.J. Cox, C.F. Bodecker, and J.H. Shaw, eds. A Survey of the Literature of Dental Caries. A Report of the Committee on Dental Health, Food and Nutrition Board, National Research Council. National Academy of Sciences, Washington, D.C.
Shaw, J.H. 1987. Causes and control of dental caries. New Engl. J. Med. 317:996-1004.
Shaw, J.H., and D. Griffiths. 1963. Dental abnormalities in rats attributable to protein deficiency during reproduction. J. Nutr. 80:123-141.
Sheiham, A. 1983. Sugars and dental decay. Lancet 1:282-284.
Sheiham, A. 1984. Changing trends in dental caries. Int. J. Epidemiol. 13:142-147.
Shrestha, B.M., and P.A. Kreutler. 1983. A comparative rat caries study on cariogenicity of foods using the intubation and gel methods. J. Dent. Res. (sp. iss.) 62:685.
Shyu, K.W., and M.Y. Hsu. 1980. The cariogenicity of xylitol, mannitol, sorbitol and sucrose. Proc. Natl. Sci. Counc., Repub. China 4:21-26.
Silverstone, L.M. 1984. The significance of remineralization in caries prevention. Can. Dent. Assoc. J. 50:157-167.
Singer, L., and R. Ophaug. 1979. Total fluoride intake of infants. Pediatrics 63:460-466.
Skinner, A., P. Connolly, and M.N. Naylor. 1982. Influence of the replacement of dietary sucrose by maltose in solid and in solution on rat caries. Caries Res. 16:443-452.
Sognnaes, R.F. 1948. Analysis of wartime reduction of dental caries in European children. Am. J. Dis. Child. 75:792-821.
Sognnaes, R.F. 1965. Fluoride protection of bones and teeth. Science 150:989-993.
Sreebny, L.M. 1982a. Sugar availability, sugar consumption and dental caries. Community Dent. Oral Epidemiol. 10:1-7.
Sreebny, L.M. 1982b. The sugar-caries axis. Int. Dent. J. 32: 1-12.
Stamm, J.W., and D.W. Banting. 1980. Comparison of root caries prevalence in adults with life-long residence in fluoridated and non-fluoridated communities. J. Dent. Res. 59:552.
Stanmeyer, W.R. 1963. The problem of dental caries in military dentistry: proceedings of the Conference on Phosphates and Dental Caries. J. Dent. Res. 43:997-998.
Strean, L.P. 1958. The importance of pyridoxine in the suppression of dental caries in school children and hamsters. N.Y. State Dent. J. 24:133-137.
Strean, L.P., E.W. Gilfillan, and G.A. Emerson. 1956. Suppressive effect of pyridoxine as dietary supplement on dental caries in Syrian hamster. N.Y. J. Dent. 22:325.
Takeuchi, M. 1961. Epidemiological study on dental caries in Japanese children, before, during and after World War II. Int. Dent. J. 11:443-457.
Tehrani, A., F. Brudevold, F. Attarzadeh, J. Van Houte, and J. Russo. 1983. Enamel demineralization by mouth rinses containing different concentrations of sucrose. J. Dent. Res. 62:1216-1217.
Tenovuo, J., K.K. Makinen, and K. Paunio. 1984. Effects on oral health of mouthrinses containing xylitol, sodium cyclamate and sucrose sweeteners in the absence of oral hygiene. IV. Analysis of whole saliva. Proc. Finn. Dent. Soc. 80.28-34.
Toverud, G. 1957. The influence of war and post-war conditions on the teeth of Norwegian school children. Milbank Mem. Fund Q. 35:373-459.
van Houte, J. 1976. Oral bacterial colonization: mechanisms and implications. Pp. 3-32 in H.M. Stiles, W.J. Loesche, and T.C. O'Brien, eds. Microbial Aspects of Dental Caries, Vol. 1. Information Retrieval, Inc., Washington, D.C.
Weatherell, J.A., D. Deutsch, C. Robinson, and A.S. Hallsworth. 1977. Assimilation of fluoride by enamel throughout the life of the tooth. Caries Res. 11 suppl. 1:85-115.