EFFECT OF DIET ON DENTAL CARIES R. L. Hartles & S. A. Leach 2. Initiation of Caries Dental caries is initiated at the interface of the enamel surface and its immediate environment, the dental plaque. The tooth surface may be breached as a result of the metabolic activity of micro-organisms in the plaque. Two major factors will determine whether or not the tooth surface becomes carious, namely the intensity of the microbiological challenge and the resistance of the tooth surface to dissolution by microbiologically produced acids.
EFFECT OF DIET ON DENTAL CARIES R. L. HARTLES Ph.D. D.Sc. S. A. LEACH B.Sc. Ph.D.
3. Factors Affecting Caries Resistance The only nutrient that has been proved to increase caries resistance is fluoride. Fluoride accumulates in surface enamel and its deposition can occur during mineralization, after mineralization is complete from the surrounding tissue fluids, and after eruption. Thefirsttwo mechanisms are systemic and the third environmental. The subject of caries resistance in relation to the chemistry of enamel is reviewed by Brudevold, McCann & Gran (1965). A detailed discussion offluorideand dental caries is presented by Jenkins (1962)2. Some attention has been given to possible associations between dental caries and water-borne trace elements other than fluoride. A number of trace elements is known to occur in enamel, especially in the outer layers (Brudevold et al. 1965). A study carried out in two isolated villages in Colombia, South America,- is worthy of note (Glass, Rothman, Espinal, V61ez & Smith, 1973). These two villages had supplies of drinkingwater each containing less than 0.1 p.p.m.fluoride.The difference in the prevalence of dental caries was such as might have been expected between areas of minimal and optimal fluoride ingestion. Analysis showed that concentrations of calcium, magnesium, molybdenum and vanadium were higher in the water samples from the village with the low caries prevalence, while concentrations of copper, iron and manganese were higher in the samples from the village with the higher prevalence. Adkins & Losee (1970) also reported that high levels of manganese and copper in drinking-water occurred in association with a high prevalence of caries. Selenium has also been indicted as a "caries-enhancing trace element" (Hadjimarkos, 1969). This is an area of study that will repay investigation. Trace elements may influence resistance of the enamel surface to dissolution.
Department of Dental Sciences School of Dental Surgery University of Liverpool 1 2 3 4 5 6 7 8 9 10 11 12 13
Nutritional factors Initiation of caries Factors affecting caries resistance Diet and dental disease Factors responsible for dental caries Carbohydrate and dental caries Some misunderstandings relating to diet and dental caries Refinement of foods and dental caries Physical properties of foods Frequency of sucrose intake and caries Sucrose and other sugars in relation to caries Other dietary components that may influence caries Conclusions References
In discussing the effect of diet on the teeth and their liability to decay it is important to distinguish between (i) truly nutritional effects on the formation and composition of the teeth and (ii) the environmental effects of dietary components on the surface of the erupted tooth and on the metabolism of the microorganisms living on the tooth surface (the dental plaque)1. 1. Nutritional Factors In man, the deciduous teeth (20 in all) begin to mineralize between four and six months in utero. Mineralization of the crowns of the incisors is completed by the first three months of life and of the canines and molars before the first year. Of the permanent teeth, the first molars begin to mineralize at birth and mineralization of the crown is completed during the third year; in the incisors and canines, mineralization begins during the first year and is completed by the age of seven. Mineralization of the premolars and second molars begins during the second year and is completed by the age of eight. Unlike bone, the teeth do not undergo remodelling; except for resorption of the roots of deciduous teeth the biological deposition of mineral is a one-way process. Further, it is extremely difficult to influence the formation of teeth by dietary means. The tooth is formed at the expense of the bones when mineral deficiencies are severe. Once the crown of the tooth is fully formed it is unlikely to be influenced by systemic means, although it may undergo minor modifications by ionic adsorption. Thus the only teeth that are likely to be influenced by systemic physiological factors beyond the age of eight are the third molars (wisdom teeth), whose mineralization may not be completed until the sixteenth year. 1
4. Diet and Dental Disease In contrast to the lack of evidence of any pre-eruptive effects of nutrition on the subsequent development of dental caries and health of their supporting structures, it can be stated beyond all reasonable doubt that certain components of the diet have a marked effect on the erupted tooth and, as such, play a significant role in the aetiology of dental caries. Dental caries in animals can be reduced virtually to nil when they are fed by stomach tube. The particular dietary components concerned are those carbohydrates capable of being fermented to acid by the bacterial aggregates localized on the sheltered surfaces of the teeth (dental plaque). Dental caries, which is characteristic of civilized man, and of which there is a clearly established, direct relation between its occurrence and living standards
ScealioHardle *Bowden, pp. 131-136 of this Bulletin.—ED.
2 Sec also Jenkins, pp. 142-145 of this Bulletin.—ED.
137 VoL3.JNicv.2w
EFFECT OF DIET ON DENTAL CARIES R. L. Hartles & S. A. Leach throughout the world, is certainly the most common dental disease affecting those in the Western world under the age of 25. The other major dental disease, i.e., periodontal disease, which is a deterioration of the supporting tissues of the teeth, becomes of great significance with increase in age and, although less fashionable in Western society in terms of desire for treatment, it is probably more extensive and more responsible for tooth loss than is dental caries. In contrast to dental caries, however, its aetiology is poorly understood at present, and there is no single dietary component that is known to play a significant role in the disease process. In fact, present evidence would suggest that such a component does not in fact exist, as its occurrence seems to be entirely indepenednt of the diet. In contrast yet again to dental caries, its world-wide prevalence is inversely rather than directly proportional to living standards. A World Workshop in Periodontics (see Hazen, 1968) concluded that nutritional deficiencies probably do not initiate periodontal disease but may modify the severity and extent of its progress by altering the resistance and repair potential of the affected local tissues. The supporting evidence for this statement, although unequivocal itself, has been derived from laboratory animals under extreme experimental conditions, and it is difficult to extrapolate these studies directly to human beings. Because of the general lack of definitive evidence to associate any aspect of human periodontal disease directly with the diet, as briefly outlined above, the remainder of this paper will be primarily concerned with the effects of diet on dental caries.
it is capable only of ionic, not structural, remodelling. Once formed and mineralized it is non-vital in the sense that it neither respirates nor regenerates. This does not mean, of course, that it is inert; it is a semipermeable membrane and minor modifications of its chemical composition and structure can occur by interaction of the components that pass through the liquid phase of its structure. Although its proportional volume is small, this phase can constitute a site of considerable activity because the small crystal size of the mineral phase provides a large surface area available for reaction. The plaque consists of an adherent mass of micro-organisms, salivary degradation products and the products of microbial metabolism. It occurs in greatest quantity in those sites on the tooth surface that are least self-cleansing—for example, in the pits andfissuresof the occlusal surfaces and between the teeth. Although food debris can often be present in these sites, it is not the debris itself that has any direct role in the carious process, but only those components that are capable of being released from it in a soluble form and are able to diffuse into the plaque and be metabolized by the bacteria. The organisms in the plaque can convert fermentable carbohydrate to organic acids, and it is these acids that, by lowering the pH locally, cause the initial breach and subsequent dissolution of the mineralized enamel. There are, therefore, three major factors required simultaneously for the production of caries: (i) a tooth surface, (ii) a dental plaque, and (iii) substrates for use by the plaque micro- organisms. The factors controlling the onset of the disease are primarily of environmental origin, but local circumstances may be influenced by the physical and chemical nature of the tooth surface and the anatomical arrangement of the teeth in the jaw. Thus it is probable that a fluoridated tooth surface will resist a given cariogenic challenge to a greater degree than a similar non-fluoridated tooth surface. The term "caries resistance" must be treated with extreme caution. Freedom from caries is not necessarily a state of caries resistance; tooth surfaces can be susceptible but spared from caries attack by the absence of a suitable challenge, so that genuine resistance is simulated. There are many examples of dental health deteriorating shortly after a community begins to live on Western foods, the best known example being the Eskimos. In Western man, the approximal surfaces of the enamel normally become carious morereadilythan the buccal or lingual surfaces without necessarily being more susceptible, as the latter surfaces are naturally self-cleansing and are exposed to a lesser challenge. If dental plaque is allowed to form on these surfaces, however, by introducing prosthetic appliances adjacent to them, they then become as susceptible to caries as the neighbouring approximal surfaces.
5. Factors Responsible for Dental Caries The easily observed fact that teeth decay at precisely those locations where food adheres and where various impactions occur has given rise, since early times, to the idea that food on the outside of the tooth causes caries. We are indebted to the classical experiments of Miller (1890) carried out towards the end of the last century for giving the first scientifically acceptable description of the carious process, when he showed that teeth could be decalcified during incubation with saliva and bread. It was also first realized at about this time that it was only the bacteria occurring locally within these impactions (gelatinous microbic plaque) that were responsible for the destruction of the tooth immediately adjacent to them and not those occurring within the oral environment in general. This latter aspect has sometimes been overlooked when over-zealous followers of Miller's fundamental ideas have either postulated explanations or made recommendations concerning the relative cariogenicity of various carbohydrate-containing food-stuffs. The initiation of the carious lesion is a surface phenomenon occurring at the interface between the enamel surface and the base of the dental plaque. The challenge to the integrity of the enamel surface is compounded of dietary and microbiological factors with considerable interactions between the two. The rate of attack is accelerated or decelerated by a multiplicity of conditions. Although the genetic template of tooth morphology can be modified in experimental animals by extreme nutritional manipulations during development, those factors that have a direct and local effect on the establishment, growth, and metabolism of the dental plaque in the human being are much more important than indirect systemic conditions in determining the initiation and progress of the dissolution of the tooth (Milhlemann, 1965). Once enamel has been formed
6. Carbohydrate and Dental Caries The two major sources of carbohydrate in contemporary Western diets are starches and sucrose in various forms. The summation of the composite information that is now available from human epidemiological studies, together with animal and laboratory experimentation of various dietary components, can justifiably incriminate sucrose as the "arch criminal" of dental caries (Newbrun, 1967). A clear distinction in cariogenicity can be made between these two sources of carbohydrate. The starches of high molecular weight are not immediately available substrates for micro-organisms; it is necessary that 138 Br. Med. Bull 1975
EFFECT OF DIET ON DENTAL CARIES K L. Hartles & S. A. Leach they be hydrolysed to smaller units before they can enter plaque. This can be done, but it takes time. The small sucrose molecule, on the other hand, provides an immediate source of substrate for the plaque bacteria. The general statement that polysaccharides (starches) arc much less cariogenic than monoand di-saccharides (sucrose) can now reasonably be said to be beyond dispute. It is only within the last decade or so, however, that the distinction between the cariogenicity of the highand low-molecular-weight carbohydrates has manifested itself so clearly. The part played in the carious process by physical consistency and degree of refinement, not only of the carbohydrates themselves, but also of the other dietary components, is still not clear (Jenkins, 1962,1966). The only way of determining the importance of these factors would be by clinical experiments in man in which large populations would be asked to live on certain rigorously controlled diets for a number of years. It would, however, be entirely unrealistic to expect significant numbers of people to change their dietary habits to the extent required to make these trials valid.
solubility of teeth in test-tube experiments, when compared with their refined counterparts, but their effectiveness in the human mouth has yet to be demonstrated (Jenkins, 1966). It must be remembered that the urbanized Bantu also began to practise the westernized habit of taking sucrose-containing products between meals. During the Second World War and the immediate post-war years there was, in several countries, a reduction in the availability of sugar and refined carbohydrate. In the United Kingdom the changes were qualitative rather than quantitative, as with the Bantu. Less sugar and highly refined flour were eaten, but the consumption of highextraction flours, potatoes and vegetables was increased The interesting fact emerged that in the United Kingdom, Scandinavia and Japan there was a progressive decrease in the prevalence of caries (Hartles, 1971). This decrease was observed until 1947-48. It was found that the reduction in caries did not occur until some years after rationing began and continued after rationing had relaxed. This information was used as evidence that something beneficial to the teeth had been removed from the food duringrefining,and it was argued that this reduction could not have resulted from an altered environment, the effect of which would have been more immediate. This interpretation has been questioned, however, on the ground that any change in the caries rate would have taken several years to produce an effect large enough to be detected and measured (Parfitt, 1954). The most likely explanation for the improvement in dental health lay in the non-availability of sugar, especially for the manufacture of confectionery for betweenmeals eating. From observations on the relation between caries incidence and dietary customs, some have put forward the view that the refining of carbohydrates, with the concomitant elimination of nutritionally valuable and protective factors, could render them more harmful to the teeth. The evidence available at present, however, although based on experiments with rats rather than studies in man, indicates that the reverse is nearer the truth. It was found (Konig, 1968) that rats fed on bread made from unrefined flour (wholemeal) have a consistently higher caries incidence than those fed on refined flour (70-82 % extraction rate). Supplementation of the refined breads with B vitamins increased rather than decreased the caries incidence, although more unsupplemented bread was eaten by the animals. The increase in cariogenicity has been attributed to the possibility that a diet of increased nutritional value to the host may also enhance the requirements for multiplication of micro-organisms. The caries incidence that is produced by all these breads, however, is small compared with that produced from sucrose, whether it be refined or not. Another misconception is that honey, because of its relative richness in vitamins and trace elements, should be good for all of the human body including the teeth. Experiments with rats have shown that it is more cariogenic than sucrose under comparable conditions (Wakeman, Smith, Zepplin, Sarles & Phillips, 1948). A statistical investigation of the caries incidence in sugarcane eaters has shown it to be high, and not low as popularly believed (Dreizien & Spies, 1952).
7. Some Misunderstandings Relating to Diet and Dental Caries It is often relatively simple with the benefit of hindsight to identify the advantages or otherwise of the course of action that has been taken by others in relation to a particular circumstance. Such is the case with the progress of research in relation to dental caries. It would now seem that certain courses of action and the results and interpretation derived from them, although carried out in good faith and with all reasonableness at the time of execution, have led to certain misunderstandings relating to diet and dental disease. Rather than reiterate in minute chronological order and detail the sequence of events that has led to the present views on these matters, it would seem that the interests of present readers would perhaps best be served by merely outlining the evidence that is available in support of these views. The subject has been reviewed by, among others, Jenkins (1962), Muhlemann (1965), Konig (1968) and Hartles (1971). 8. Refinement of Foods and Dental Caries Before the intervention of Western man, the Eskimos lived on a diet that was virtually free from carbohydrate and possessed dentitions almost free from dental caries. When their diet was partly replaced by carbohydrate foods, the prevalence of caries increased markedly. No decisive conclusion can be drawn from this, as there was a concomitant reduction in fat, fat-soluble vitamins and protein, and possibly other more elusive differences (Jenkins, 1966). It was found that the caries incidence among the South African Bantu was higher among town-dwellers living on westernized food than among similar groups living in their native kraals. The situation was entirely different from that of the Eskimos, however, as in this instance the amount of carbohydrate eaten by both urban and rural groups was comparable; the urbanized Bantu had seemingly merely exchanged his unrefined foods (mealie meal) for refined products (white bread and refined sugar). It was suggested that the refinement of carbohydrate foods removed protective factors from them, and laboratory experiments carried out on the dissolution of whole teeth incubated in saliva confirmed this view (Osborn, Noriskin & Staz, 1937). There is no doubt that unrefined flours and crude cane juice do contain substances that reduce the
9. Physical Properties of Foods It has long been believed that hard and coarse foods can exert a detergent action during mastication that is valuable in preventing caries. It is argued that the increase in salivary flow 139
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EFFECT OF DIET ON DENTAL CARIES R: L. Hartles & S. A. Leach which these foods stimulate should help either toflushaway or to neutralize undesirable material adjacent to and within the dental plaque, and in addition should exert a cleansing effect on smooth surfaces by direct mechanical friction. These processes must certainly take place in the mouth to some degree, but the actual contribution they make is far from clear. Although, . in dental health education, the importance of detergent foods is emphasized, it is surprising that few experiments have produced results that support this belief. One experiment was carried out for two years with about 200 children, in which it was found that the group that ate hard apples after meals showed a smaller but not statistically significant increase in caries incidence than did the controls (Slack & Martin, 1958). No comments were made on the amount of plaque formed. We have found in our own laboratories that the chewing of excessive amounts (1 kg) of either hard apples or raw carrots over a period of an hour removed plaque from the easily accessible upper two-thirds of the teeth but had no effect on the less available plaque located in the approximal surfaces or adjacent to the gingival margins. The surfaces that were cleaned were those that are normally virtually free from dental caries. The almost ubiquitous occurrence of gingival plaque and of periodontal disease in man, throughout the whole range of hard and soft diets, presumably means that diet consistency per se cannot control the production and establishment of plaque in these areas (Leach, 1971). Apples, although perhaps without effect on plaque removal directly, have been shown to remove food particles and accelerate the clearance of sugar from the mouth. They could also have a much more significant role in reducing caries if they could be used to blunt the appetite for sweets and confectionery, as also could all the other fibrous foods such as raw carrots and celery. It must be noted, however, that half an apple eaten immediately before retiring to bed lowers the plaque pH to critical levels for three hours afterwards (Graf, 1970). Salivary flow is markedly reduced during sleep. It has sometimes been suggested that one effect of a hard and coarse diet would be to wear away the cusps of the teeth and so make them shallower and self-cleansing. Occlusal caries of the molars in modern times begins within three years of eruption. A study of the skulls of Anglo-Saxon man, who lived on a coarse diet and had a caries incidence less than in any other period studied in England, indicated that the amount of attrition in three years hardly altered the form of the molar fissures, which were not completely worn away even 14 years after eruption (Hardwick, 1960). 10. Frequency of Sucrose Intake and Caries A survey of the dental literature carried out in 1953 indicated that attempts to correlate sugar intake to the incidence of caries had led to contradictory results (Gustafsson, 1954). Direct evidence of an association between sugar consumption and caries has since been provided by a study of over 400 institutionaJized patients at Vipeholm in Sweden (Gustafsson, Quensel, Lanke, Lundqvist, Grahn6n, Bonow & Krasse, 1954). The findings indicated that an increased consumption of sugar could result in an increase in caries, but the effect depended not only on the quantity of sugar consumed but also on the manner of its administration. When the extra sugar was taken solely at meal-times it had little or no effect on subsequent caries. The greatest increase occurred in patients who consumed sugary confections between meals, and in this respect toffees and
caramels were more cariogenic than chocolate. Thus, the important finding was a direct correlation between increased caries and the consumption of sugar between meals. This finding has now helped to remove many of the apparent contradictions that had existed in previous work relating sugar consumption to caries incidence. Some recent work using a telemetric recording device has shown that the pH of the plaque drops to a critical level for a total of three hours each day if sugar is taken only at meal-times, whereas the consumption of sugar between meals keeps the plaque pH below the critical level for eight hours (Graf, 1970). These results seem to explain the results of the Vipeholm study and lend strong support to the acidogenic theory of dental caries. 11. Sucrose and Other Sugars in Relation to Caries There is enough evidence to establish a prima facie case that sucrose is potentially the dietary component most harmful to the teeth, especially when consumed between meals. These findings, however, do not permit any conclusions to be drawn concerning the specific cariogenicity of sucrose. They merely indicate that a small-molecular-weight carbohydrate such as sucrose is cariogenic. It is now necessary to ask whether sucrose assumes importance in the promotion of dental caries merely because it happens to be the only common sugar consumed in large quantity, or whether it has specific properties that render it uniquely more harmful than other sugars. If the former were the case, then substitution of, say, glucose for sucrose would have no beneficial effect. If the latter were true, replacement of sucrose by other sugars might be beneficial (Leach, 1969). It would not, of course, be morally justifiable to find answers to these questions by deliberately attempting to increase caries in children by dietary means. Animal experimentation, however, has indicated that all the small-molecular-weight carbohydrates are highly cariogenic, compared with starch. Some of the better controlled studies have shown that sucrose is sometimes marginally the most cariogenic and that its cariogenicity is directly related to the frequency of eating (Konig, 1968; Green & Hartles, 1969). 12. Other Dietary Components that may Influence Caries i. Fatt. Evidence from the rat (Green & Hartles, 1966) showed a significant fall in dental caries when 5 % of groundnut oil was included in a high-sucrose diet. These workers also showed that fat-soluble vitamins were without effect on caries incidence in the rat. ii. Water-soluble vitamins. There is no evidence to suggest that a diet rich in any of the water-soluble vitamins reduces the incidence of caries. In the rat a diet grossly deficient in B vitamins does effect a reduction in caries, partly because rats do not eat so readily and probably because the micro-organisms of the plaque are also affected by lack of vitamins (Green & Hartles, 1966). iii. Sweetened syrups. It is not uncommon for infants to be given "comforters" or small "feeders" containing sweetened drinks or sugary vitaminized syrups. The adoption of this practice exposes the deciduous teeth to a potentially cariogenic environment for prolonged periods, and as such is to be deprecated. This is not a condemnation of vitamin syrups but of one means of their application. Such preparations doubtless have their value when the diet may be otherwise
140
Br. Med. Bull. 1975
EFFECT OF DIET ON DENTAL CARIES R. L. Hartles & S. A. Leach forces. The one proved method of increasing the tooth's resistance to caries is by the appropriate administration of fluoride. At a population level, the only satisfactory way of achieving this is by fluoridation of the drinking-water. Control of adverse effects in the tooth's environment may be attempted through dietary measures by reducing the frequency of eating, especially of between-meal sugary confections, thereby reducing the supply of easily fermentable carbohydrate that can be converted to acids within the dental plaque. The two approaches are complementary; their implementation would, after a number of years, be expected to reduce the incidence of dental caries significantly, probably by at least 50 %.
deficient, but there is no evidence that they have any beneficial effect in reducing the incidence of caries. 13.
Conclusions
Dental caries occurs when the equilibrium at the interface between the tooth surface and its immediate environment is disturbed, i.e., when those factors that cause the disease overcome the resistance of the tooth to local dissolution. Hence, there are two ways in which it is possible to control the disease: by increasing the resistance of the tooth surface or by reducing the potency of the environmental and microbiological
REFERENCES
Adkins, B. L. & Losee, F. L. (1970) New York State Dent. J. 36, 618-622 Brudevold, F., McCann, H. G. & Gren, P. (1965) In: Wolstenholme, G. E. W. & O'Connor, M., cd. Cartes-resistant teeth, pp. 121-140 (Ciba Foundation symposium). Churchill, London Dreizen, S. & Spies, T. D. (1952) / . Am. Dent. Assoc. 45,193-200 Glass, R. L., Rothman, K. J., Espinal, F., V61ez, H. & Smith, N. J. (1973) Arch. Oral Biol. 18,1099-1104 Graf, H. (1970) Int. Dent. J. 20,426-435 Green, R. M. & Hartles, R. L. (1966) Arch. Oral Biol. 11,913-919 Green, R. M. & Hartles, R. L. (1969) Arch. Oral Biol. 14,235-241 Gustafsson, B. E. (1954) Ada Odontol. Scand. 11,207-231 Gustafsson, B. E., Quensel, C. E., Lanke, L. S., Lundqvist, C , Grahnen, H., Bonow, B. E. & Krasse, B. (1954) Acta Odontol. Scand. 11,232-364 Hadjimarkos, D. M. (1969) Caries Res. 3,14-22 Hardwick, J. L. (I960) Br. Dent. J. 108, 9-17 Hartles, R. L. (1971) In: Yudkin, J., Edelman J. & Hough, L., ed. Sugar, pp. 221-230. Butterworths, London
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Hazen, S. P. (1968) Alabama J. Med. Sci. 5, 328-335 Jenkins, G. N. (1962) In: Sognnaes, R. F., cd. Chemistry and prevention of caries, pp. 126-163. Thomas, Springfield, IH. Jenkins, G. N. (1966) Adv. Oral Biol. 2, 67-100 Konig, K. G. (1968) Alabama J. Med. Sci. 5,269-275 Leach, S. A. (1969) Br. Dent. J. 127, 325-330 Leach, S. A. (1971) In: Eastoe, J. E., Picton, D. C. A. & Alexander, G. A., ed. The prevention of periodontal disease, pp. 136-138. Kimpton, London Miller, W. D. (1890) The micro-organisms of the human mouth, p. 208. White, Philadelphia, Pa Muhlemann, H. R. (1965) In: Blix, G., ed. Nutrition and cariesprevention, pp. 9-19. Almqvist & Wiksell, Uppsala Newbrun, E. (1967) Odontol. Revy, 18, 373-386 Osborn, T. W. B., Noriskin, J. N. & Staz, J. (1937) / . Dent. Res. 16,165-171 Parfitt, G. J. (1954) Br. Dent. J. 97, 235-237 Slack, G. L. & Martin, W. J. (1958) Br. Dent. J. 105,366-371 Wakeman, E. J., Smith, J. K., Zepplin, M., Sarles, W. B. & Phillips, P. H. (1948) / . Dent. Res. 27,489-492
EFFECT OF DIET ON DENTAL CARIES R. L. HARTLES Ph.D. D.Sc. S. A. LEACH B.Sc. Ph.D.
3. Factors Affecting Caries Resistance The only nutrient that has been proved to increase caries resistance is fluoride. Fluoride accumulates in surface enamel and its deposition can occur during mineralization, after mineralization is complete from the surrounding tissue fluids, and after eruption. Thefirsttwo mechanisms are systemic and the third environmental. The subject of caries resistance in relation to the chemistry of enamel is reviewed by Brudevold, McCann & Gran (1965). A detailed discussion offluorideand dental caries is presented by Jenkins (1962)2. Some attention has been given to possible associations between dental caries and water-borne trace elements other than fluoride. A number of trace elements is known to occur in enamel, especially in the outer layers (Brudevold et al. 1965). A study carried out in two isolated villages in Colombia, South America,- is worthy of note (Glass, Rothman, Espinal, V61ez & Smith, 1973). These two villages had supplies of drinkingwater each containing less than 0.1 p.p.m.fluoride.The difference in the prevalence of dental caries was such as might have been expected between areas of minimal and optimal fluoride ingestion. Analysis showed that concentrations of calcium, magnesium, molybdenum and vanadium were higher in the water samples from the village with the low caries prevalence, while concentrations of copper, iron and manganese were higher in the samples from the village with the higher prevalence. Adkins & Losee (1970) also reported that high levels of manganese and copper in drinking-water occurred in association with a high prevalence of caries. Selenium has also been indicted as a "caries-enhancing trace element" (Hadjimarkos, 1969). This is an area of study that will repay investigation. Trace elements may influence resistance of the enamel surface to dissolution.
Department of Dental Sciences School of Dental Surgery University of Liverpool 1 2 3 4 5 6 7 8 9 10 11 12 13
Nutritional factors Initiation of caries Factors affecting caries resistance Diet and dental disease Factors responsible for dental caries Carbohydrate and dental caries Some misunderstandings relating to diet and dental caries Refinement of foods and dental caries Physical properties of foods Frequency of sucrose intake and caries Sucrose and other sugars in relation to caries Other dietary components that may influence caries Conclusions References
In discussing the effect of diet on the teeth and their liability to decay it is important to distinguish between (i) truly nutritional effects on the formation and composition of the teeth and (ii) the environmental effects of dietary components on the surface of the erupted tooth and on the metabolism of the microorganisms living on the tooth surface (the dental plaque)1. 1. Nutritional Factors In man, the deciduous teeth (20 in all) begin to mineralize between four and six months in utero. Mineralization of the crowns of the incisors is completed by the first three months of life and of the canines and molars before the first year. Of the permanent teeth, the first molars begin to mineralize at birth and mineralization of the crown is completed during the third year; in the incisors and canines, mineralization begins during the first year and is completed by the age of seven. Mineralization of the premolars and second molars begins during the second year and is completed by the age of eight. Unlike bone, the teeth do not undergo remodelling; except for resorption of the roots of deciduous teeth the biological deposition of mineral is a one-way process. Further, it is extremely difficult to influence the formation of teeth by dietary means. The tooth is formed at the expense of the bones when mineral deficiencies are severe. Once the crown of the tooth is fully formed it is unlikely to be influenced by systemic means, although it may undergo minor modifications by ionic adsorption. Thus the only teeth that are likely to be influenced by systemic physiological factors beyond the age of eight are the third molars (wisdom teeth), whose mineralization may not be completed until the sixteenth year. 1
4. Diet and Dental Disease In contrast to the lack of evidence of any pre-eruptive effects of nutrition on the subsequent development of dental caries and health of their supporting structures, it can be stated beyond all reasonable doubt that certain components of the diet have a marked effect on the erupted tooth and, as such, play a significant role in the aetiology of dental caries. Dental caries in animals can be reduced virtually to nil when they are fed by stomach tube. The particular dietary components concerned are those carbohydrates capable of being fermented to acid by the bacterial aggregates localized on the sheltered surfaces of the teeth (dental plaque). Dental caries, which is characteristic of civilized man, and of which there is a clearly established, direct relation between its occurrence and living standards
ScealioHardle *Bowden, pp. 131-136 of this Bulletin.—ED.
2 Sec also Jenkins, pp. 142-145 of this Bulletin.—ED.
137 VoL3.JNicv.2w
EFFECT OF DIET ON DENTAL CARIES R. L. Hartles & S. A. Leach throughout the world, is certainly the most common dental disease affecting those in the Western world under the age of 25. The other major dental disease, i.e., periodontal disease, which is a deterioration of the supporting tissues of the teeth, becomes of great significance with increase in age and, although less fashionable in Western society in terms of desire for treatment, it is probably more extensive and more responsible for tooth loss than is dental caries. In contrast to dental caries, however, its aetiology is poorly understood at present, and there is no single dietary component that is known to play a significant role in the disease process. In fact, present evidence would suggest that such a component does not in fact exist, as its occurrence seems to be entirely indepenednt of the diet. In contrast yet again to dental caries, its world-wide prevalence is inversely rather than directly proportional to living standards. A World Workshop in Periodontics (see Hazen, 1968) concluded that nutritional deficiencies probably do not initiate periodontal disease but may modify the severity and extent of its progress by altering the resistance and repair potential of the affected local tissues. The supporting evidence for this statement, although unequivocal itself, has been derived from laboratory animals under extreme experimental conditions, and it is difficult to extrapolate these studies directly to human beings. Because of the general lack of definitive evidence to associate any aspect of human periodontal disease directly with the diet, as briefly outlined above, the remainder of this paper will be primarily concerned with the effects of diet on dental caries.
it is capable only of ionic, not structural, remodelling. Once formed and mineralized it is non-vital in the sense that it neither respirates nor regenerates. This does not mean, of course, that it is inert; it is a semipermeable membrane and minor modifications of its chemical composition and structure can occur by interaction of the components that pass through the liquid phase of its structure. Although its proportional volume is small, this phase can constitute a site of considerable activity because the small crystal size of the mineral phase provides a large surface area available for reaction. The plaque consists of an adherent mass of micro-organisms, salivary degradation products and the products of microbial metabolism. It occurs in greatest quantity in those sites on the tooth surface that are least self-cleansing—for example, in the pits andfissuresof the occlusal surfaces and between the teeth. Although food debris can often be present in these sites, it is not the debris itself that has any direct role in the carious process, but only those components that are capable of being released from it in a soluble form and are able to diffuse into the plaque and be metabolized by the bacteria. The organisms in the plaque can convert fermentable carbohydrate to organic acids, and it is these acids that, by lowering the pH locally, cause the initial breach and subsequent dissolution of the mineralized enamel. There are, therefore, three major factors required simultaneously for the production of caries: (i) a tooth surface, (ii) a dental plaque, and (iii) substrates for use by the plaque micro- organisms. The factors controlling the onset of the disease are primarily of environmental origin, but local circumstances may be influenced by the physical and chemical nature of the tooth surface and the anatomical arrangement of the teeth in the jaw. Thus it is probable that a fluoridated tooth surface will resist a given cariogenic challenge to a greater degree than a similar non-fluoridated tooth surface. The term "caries resistance" must be treated with extreme caution. Freedom from caries is not necessarily a state of caries resistance; tooth surfaces can be susceptible but spared from caries attack by the absence of a suitable challenge, so that genuine resistance is simulated. There are many examples of dental health deteriorating shortly after a community begins to live on Western foods, the best known example being the Eskimos. In Western man, the approximal surfaces of the enamel normally become carious morereadilythan the buccal or lingual surfaces without necessarily being more susceptible, as the latter surfaces are naturally self-cleansing and are exposed to a lesser challenge. If dental plaque is allowed to form on these surfaces, however, by introducing prosthetic appliances adjacent to them, they then become as susceptible to caries as the neighbouring approximal surfaces.
5. Factors Responsible for Dental Caries The easily observed fact that teeth decay at precisely those locations where food adheres and where various impactions occur has given rise, since early times, to the idea that food on the outside of the tooth causes caries. We are indebted to the classical experiments of Miller (1890) carried out towards the end of the last century for giving the first scientifically acceptable description of the carious process, when he showed that teeth could be decalcified during incubation with saliva and bread. It was also first realized at about this time that it was only the bacteria occurring locally within these impactions (gelatinous microbic plaque) that were responsible for the destruction of the tooth immediately adjacent to them and not those occurring within the oral environment in general. This latter aspect has sometimes been overlooked when over-zealous followers of Miller's fundamental ideas have either postulated explanations or made recommendations concerning the relative cariogenicity of various carbohydrate-containing food-stuffs. The initiation of the carious lesion is a surface phenomenon occurring at the interface between the enamel surface and the base of the dental plaque. The challenge to the integrity of the enamel surface is compounded of dietary and microbiological factors with considerable interactions between the two. The rate of attack is accelerated or decelerated by a multiplicity of conditions. Although the genetic template of tooth morphology can be modified in experimental animals by extreme nutritional manipulations during development, those factors that have a direct and local effect on the establishment, growth, and metabolism of the dental plaque in the human being are much more important than indirect systemic conditions in determining the initiation and progress of the dissolution of the tooth (Milhlemann, 1965). Once enamel has been formed
6. Carbohydrate and Dental Caries The two major sources of carbohydrate in contemporary Western diets are starches and sucrose in various forms. The summation of the composite information that is now available from human epidemiological studies, together with animal and laboratory experimentation of various dietary components, can justifiably incriminate sucrose as the "arch criminal" of dental caries (Newbrun, 1967). A clear distinction in cariogenicity can be made between these two sources of carbohydrate. The starches of high molecular weight are not immediately available substrates for micro-organisms; it is necessary that 138 Br. Med. Bull 1975
EFFECT OF DIET ON DENTAL CARIES K L. Hartles & S. A. Leach they be hydrolysed to smaller units before they can enter plaque. This can be done, but it takes time. The small sucrose molecule, on the other hand, provides an immediate source of substrate for the plaque bacteria. The general statement that polysaccharides (starches) arc much less cariogenic than monoand di-saccharides (sucrose) can now reasonably be said to be beyond dispute. It is only within the last decade or so, however, that the distinction between the cariogenicity of the highand low-molecular-weight carbohydrates has manifested itself so clearly. The part played in the carious process by physical consistency and degree of refinement, not only of the carbohydrates themselves, but also of the other dietary components, is still not clear (Jenkins, 1962,1966). The only way of determining the importance of these factors would be by clinical experiments in man in which large populations would be asked to live on certain rigorously controlled diets for a number of years. It would, however, be entirely unrealistic to expect significant numbers of people to change their dietary habits to the extent required to make these trials valid.
solubility of teeth in test-tube experiments, when compared with their refined counterparts, but their effectiveness in the human mouth has yet to be demonstrated (Jenkins, 1966). It must be remembered that the urbanized Bantu also began to practise the westernized habit of taking sucrose-containing products between meals. During the Second World War and the immediate post-war years there was, in several countries, a reduction in the availability of sugar and refined carbohydrate. In the United Kingdom the changes were qualitative rather than quantitative, as with the Bantu. Less sugar and highly refined flour were eaten, but the consumption of highextraction flours, potatoes and vegetables was increased The interesting fact emerged that in the United Kingdom, Scandinavia and Japan there was a progressive decrease in the prevalence of caries (Hartles, 1971). This decrease was observed until 1947-48. It was found that the reduction in caries did not occur until some years after rationing began and continued after rationing had relaxed. This information was used as evidence that something beneficial to the teeth had been removed from the food duringrefining,and it was argued that this reduction could not have resulted from an altered environment, the effect of which would have been more immediate. This interpretation has been questioned, however, on the ground that any change in the caries rate would have taken several years to produce an effect large enough to be detected and measured (Parfitt, 1954). The most likely explanation for the improvement in dental health lay in the non-availability of sugar, especially for the manufacture of confectionery for betweenmeals eating. From observations on the relation between caries incidence and dietary customs, some have put forward the view that the refining of carbohydrates, with the concomitant elimination of nutritionally valuable and protective factors, could render them more harmful to the teeth. The evidence available at present, however, although based on experiments with rats rather than studies in man, indicates that the reverse is nearer the truth. It was found (Konig, 1968) that rats fed on bread made from unrefined flour (wholemeal) have a consistently higher caries incidence than those fed on refined flour (70-82 % extraction rate). Supplementation of the refined breads with B vitamins increased rather than decreased the caries incidence, although more unsupplemented bread was eaten by the animals. The increase in cariogenicity has been attributed to the possibility that a diet of increased nutritional value to the host may also enhance the requirements for multiplication of micro-organisms. The caries incidence that is produced by all these breads, however, is small compared with that produced from sucrose, whether it be refined or not. Another misconception is that honey, because of its relative richness in vitamins and trace elements, should be good for all of the human body including the teeth. Experiments with rats have shown that it is more cariogenic than sucrose under comparable conditions (Wakeman, Smith, Zepplin, Sarles & Phillips, 1948). A statistical investigation of the caries incidence in sugarcane eaters has shown it to be high, and not low as popularly believed (Dreizien & Spies, 1952).
7. Some Misunderstandings Relating to Diet and Dental Caries It is often relatively simple with the benefit of hindsight to identify the advantages or otherwise of the course of action that has been taken by others in relation to a particular circumstance. Such is the case with the progress of research in relation to dental caries. It would now seem that certain courses of action and the results and interpretation derived from them, although carried out in good faith and with all reasonableness at the time of execution, have led to certain misunderstandings relating to diet and dental disease. Rather than reiterate in minute chronological order and detail the sequence of events that has led to the present views on these matters, it would seem that the interests of present readers would perhaps best be served by merely outlining the evidence that is available in support of these views. The subject has been reviewed by, among others, Jenkins (1962), Muhlemann (1965), Konig (1968) and Hartles (1971). 8. Refinement of Foods and Dental Caries Before the intervention of Western man, the Eskimos lived on a diet that was virtually free from carbohydrate and possessed dentitions almost free from dental caries. When their diet was partly replaced by carbohydrate foods, the prevalence of caries increased markedly. No decisive conclusion can be drawn from this, as there was a concomitant reduction in fat, fat-soluble vitamins and protein, and possibly other more elusive differences (Jenkins, 1966). It was found that the caries incidence among the South African Bantu was higher among town-dwellers living on westernized food than among similar groups living in their native kraals. The situation was entirely different from that of the Eskimos, however, as in this instance the amount of carbohydrate eaten by both urban and rural groups was comparable; the urbanized Bantu had seemingly merely exchanged his unrefined foods (mealie meal) for refined products (white bread and refined sugar). It was suggested that the refinement of carbohydrate foods removed protective factors from them, and laboratory experiments carried out on the dissolution of whole teeth incubated in saliva confirmed this view (Osborn, Noriskin & Staz, 1937). There is no doubt that unrefined flours and crude cane juice do contain substances that reduce the
9. Physical Properties of Foods It has long been believed that hard and coarse foods can exert a detergent action during mastication that is valuable in preventing caries. It is argued that the increase in salivary flow 139
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EFFECT OF DIET ON DENTAL CARIES R: L. Hartles & S. A. Leach which these foods stimulate should help either toflushaway or to neutralize undesirable material adjacent to and within the dental plaque, and in addition should exert a cleansing effect on smooth surfaces by direct mechanical friction. These processes must certainly take place in the mouth to some degree, but the actual contribution they make is far from clear. Although, . in dental health education, the importance of detergent foods is emphasized, it is surprising that few experiments have produced results that support this belief. One experiment was carried out for two years with about 200 children, in which it was found that the group that ate hard apples after meals showed a smaller but not statistically significant increase in caries incidence than did the controls (Slack & Martin, 1958). No comments were made on the amount of plaque formed. We have found in our own laboratories that the chewing of excessive amounts (1 kg) of either hard apples or raw carrots over a period of an hour removed plaque from the easily accessible upper two-thirds of the teeth but had no effect on the less available plaque located in the approximal surfaces or adjacent to the gingival margins. The surfaces that were cleaned were those that are normally virtually free from dental caries. The almost ubiquitous occurrence of gingival plaque and of periodontal disease in man, throughout the whole range of hard and soft diets, presumably means that diet consistency per se cannot control the production and establishment of plaque in these areas (Leach, 1971). Apples, although perhaps without effect on plaque removal directly, have been shown to remove food particles and accelerate the clearance of sugar from the mouth. They could also have a much more significant role in reducing caries if they could be used to blunt the appetite for sweets and confectionery, as also could all the other fibrous foods such as raw carrots and celery. It must be noted, however, that half an apple eaten immediately before retiring to bed lowers the plaque pH to critical levels for three hours afterwards (Graf, 1970). Salivary flow is markedly reduced during sleep. It has sometimes been suggested that one effect of a hard and coarse diet would be to wear away the cusps of the teeth and so make them shallower and self-cleansing. Occlusal caries of the molars in modern times begins within three years of eruption. A study of the skulls of Anglo-Saxon man, who lived on a coarse diet and had a caries incidence less than in any other period studied in England, indicated that the amount of attrition in three years hardly altered the form of the molar fissures, which were not completely worn away even 14 years after eruption (Hardwick, 1960). 10. Frequency of Sucrose Intake and Caries A survey of the dental literature carried out in 1953 indicated that attempts to correlate sugar intake to the incidence of caries had led to contradictory results (Gustafsson, 1954). Direct evidence of an association between sugar consumption and caries has since been provided by a study of over 400 institutionaJized patients at Vipeholm in Sweden (Gustafsson, Quensel, Lanke, Lundqvist, Grahn6n, Bonow & Krasse, 1954). The findings indicated that an increased consumption of sugar could result in an increase in caries, but the effect depended not only on the quantity of sugar consumed but also on the manner of its administration. When the extra sugar was taken solely at meal-times it had little or no effect on subsequent caries. The greatest increase occurred in patients who consumed sugary confections between meals, and in this respect toffees and
caramels were more cariogenic than chocolate. Thus, the important finding was a direct correlation between increased caries and the consumption of sugar between meals. This finding has now helped to remove many of the apparent contradictions that had existed in previous work relating sugar consumption to caries incidence. Some recent work using a telemetric recording device has shown that the pH of the plaque drops to a critical level for a total of three hours each day if sugar is taken only at meal-times, whereas the consumption of sugar between meals keeps the plaque pH below the critical level for eight hours (Graf, 1970). These results seem to explain the results of the Vipeholm study and lend strong support to the acidogenic theory of dental caries. 11. Sucrose and Other Sugars in Relation to Caries There is enough evidence to establish a prima facie case that sucrose is potentially the dietary component most harmful to the teeth, especially when consumed between meals. These findings, however, do not permit any conclusions to be drawn concerning the specific cariogenicity of sucrose. They merely indicate that a small-molecular-weight carbohydrate such as sucrose is cariogenic. It is now necessary to ask whether sucrose assumes importance in the promotion of dental caries merely because it happens to be the only common sugar consumed in large quantity, or whether it has specific properties that render it uniquely more harmful than other sugars. If the former were the case, then substitution of, say, glucose for sucrose would have no beneficial effect. If the latter were true, replacement of sucrose by other sugars might be beneficial (Leach, 1969). It would not, of course, be morally justifiable to find answers to these questions by deliberately attempting to increase caries in children by dietary means. Animal experimentation, however, has indicated that all the small-molecular-weight carbohydrates are highly cariogenic, compared with starch. Some of the better controlled studies have shown that sucrose is sometimes marginally the most cariogenic and that its cariogenicity is directly related to the frequency of eating (Konig, 1968; Green & Hartles, 1969). 12. Other Dietary Components that may Influence Caries i. Fatt. Evidence from the rat (Green & Hartles, 1966) showed a significant fall in dental caries when 5 % of groundnut oil was included in a high-sucrose diet. These workers also showed that fat-soluble vitamins were without effect on caries incidence in the rat. ii. Water-soluble vitamins. There is no evidence to suggest that a diet rich in any of the water-soluble vitamins reduces the incidence of caries. In the rat a diet grossly deficient in B vitamins does effect a reduction in caries, partly because rats do not eat so readily and probably because the micro-organisms of the plaque are also affected by lack of vitamins (Green & Hartles, 1966). iii. Sweetened syrups. It is not uncommon for infants to be given "comforters" or small "feeders" containing sweetened drinks or sugary vitaminized syrups. The adoption of this practice exposes the deciduous teeth to a potentially cariogenic environment for prolonged periods, and as such is to be deprecated. This is not a condemnation of vitamin syrups but of one means of their application. Such preparations doubtless have their value when the diet may be otherwise
140
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EFFECT OF DIET ON DENTAL CARIES R. L. Hartles & S. A. Leach forces. The one proved method of increasing the tooth's resistance to caries is by the appropriate administration of fluoride. At a population level, the only satisfactory way of achieving this is by fluoridation of the drinking-water. Control of adverse effects in the tooth's environment may be attempted through dietary measures by reducing the frequency of eating, especially of between-meal sugary confections, thereby reducing the supply of easily fermentable carbohydrate that can be converted to acids within the dental plaque. The two approaches are complementary; their implementation would, after a number of years, be expected to reduce the incidence of dental caries significantly, probably by at least 50 %.
deficient, but there is no evidence that they have any beneficial effect in reducing the incidence of caries. 13.
Conclusions
Dental caries occurs when the equilibrium at the interface between the tooth surface and its immediate environment is disturbed, i.e., when those factors that cause the disease overcome the resistance of the tooth to local dissolution. Hence, there are two ways in which it is possible to control the disease: by increasing the resistance of the tooth surface or by reducing the potency of the environmental and microbiological
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Hazen, S. P. (1968) Alabama J. Med. Sci. 5, 328-335 Jenkins, G. N. (1962) In: Sognnaes, R. F., cd. Chemistry and prevention of caries, pp. 126-163. Thomas, Springfield, IH. Jenkins, G. N. (1966) Adv. Oral Biol. 2, 67-100 Konig, K. G. (1968) Alabama J. Med. Sci. 5,269-275 Leach, S. A. (1969) Br. Dent. J. 127, 325-330 Leach, S. A. (1971) In: Eastoe, J. E., Picton, D. C. A. & Alexander, G. A., ed. The prevention of periodontal disease, pp. 136-138. Kimpton, London Miller, W. D. (1890) The micro-organisms of the human mouth, p. 208. White, Philadelphia, Pa Muhlemann, H. R. (1965) In: Blix, G., ed. Nutrition and cariesprevention, pp. 9-19. Almqvist & Wiksell, Uppsala Newbrun, E. (1967) Odontol. Revy, 18, 373-386 Osborn, T. W. B., Noriskin, J. N. & Staz, J. (1937) / . Dent. Res. 16,165-171 Parfitt, G. J. (1954) Br. Dent. J. 97, 235-237 Slack, G. L. & Martin, W. J. (1958) Br. Dent. J. 105,366-371 Wakeman, E. J., Smith, J. K., Zepplin, M., Sarles, W. B. & Phillips, P. H. (1948) / . Dent. Res. 27,489-492
