Journal of Human Nutrition (1979) 3 3 , 98-110.
1: Aetiology of dental disease and theoretical aspects of dietary control
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N. W. JOHNSON, MDSc, PhD, FDS, FRACDS, MRCPath Department of Oral Pathology, The London Hospital Medical College, Turner Street, London E 1 2AD, England. The term ‘dental disease’ should be taken to include both dental caries and periodontal disease for both are almost universally prevalent, both result in substantial tooth loss and both have a common cause, namely dental plaque. Because this symposium is concerned with dental disease in children it is inevitable that our discussion will be dominated by caries. This is because caries activity is highest in childhood and adolescence and it is not normally until adulthood that periodontal disease has advanced sufficiently to become a significant cause of discomfort to the patient or a major cause of tooth loss. Nevertheless both disease processes commence early in life and patterns of diet and oral hygiene, which so strongly influence the rate of progress of disease, are established at this time. Definition of dental caries Dental caries is a form of progressive destruction of enamel, dentine and cementum initiated by microbial activity at the tooth surface. In short, certain types of bacteria preferentially colonise certain sites on the tooth surface which are protected from the natural cleansing movements of the lips, cheeks and tongue and accumulate to form dental plaque. These bacteria metabolise dietary constituents, notably carbohydrate and sucrose in particular, to form organic acids. The acids are held close to the tooth surface by the relative impermeability of the plaque and are thus protected from the diluting and buffering affects of saliva. The acids so formed have an opportunity to dissolve tooth substance and this occurs slowly, intermittently, and in depth. Destruction of tissue is characteristically preceded by softening, brought about by partial dissolution of mineral ahead of the final destruction of the organic matrix of the tissue and residual mineral. Because of the characteristic pattern of alteration in depth, caries can be distinguished from other destructive processes of the crowns of the teeth such as abrasion due to mechanical wear and erosion due t o strongly acidic fluids which remove completely thin layers of the surface. Definition of periodontal disease Though there are specific forms of periodontal disease associated with specific infections and with certain systemic diseases which depress the host defence mechanisms, the unqualified term ‘periodontal disease’ refers to the presence of progressive, destructive inflammatory lesions of the tissues surrounding the teeth. These lesions are also initiated by the presence of dental plaque, residing on the tooth surface in contact with gingival soft tissue. The tissues are damaged by the direct effect of toxins and enzymes liberated by plaque microorganisms. These agents diffuse into the tissues where they also provoke inflammation. 98
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Furthermore, many plaque products, such as the lipopolysaccharide endotoxins of Gram-negative bacteria and the lipoteichoic acids of Gram-positive bacteria are antigenic, so that immunological reactions are provoked in the tissue. The immune inflammatory response, if sustained over a substantial period of time due to the continued presence of plaque, itself results in tissue damage; this is mediated by lytic enzymes released from polymorphs and macrophages and by hypersensitivity reactions of both the humoral and cell-mediated types (Cowley & MacPhee, 1975; Schluger, Yuodalis & Page, 1977). The earliest sign of periodontal disease is marginal gingivitis, ie inflammation of the gum margins. This stage of the disease is reversible, but once destruction has extended into the periodontal ligament which attaches the tooth root t o the surrounding bone, some permanent loss of tooth support is inevitable. The problem of dental disease Dental caries and periodontal disease are the most common diseases affecting Western man, with a prevalence of almost 100 per cent. In England and Wales a national survey of adults conducted in 1968 found only three people in 1000 with 28 or more teeth present and free from caries. In Britain 25 per cent of all teeth erupted in children up t o 1 2 years of age have been affected by caries; by the age of 15 this has risen to 33 per cent and by age 30, to 67 per cent. The Survey of Children’s Dental Health in England & Wales 1973 (Todd et aZ., 1975) revealed a total number of decayed, missing and filled teeth of 3.9 at age six, 5.0 at age eight and 8.4 at age 15. Many workers believe that destructive periodontal disease begins in childhood, but that it may not be recognised until the third decade, after irreversible changes have occurred (Stallard, 1967). Certainly after the age of 35 Periodontal disease becomes the major cause of tooth loss (Pelton, Pennel & Druzina, 1954). Though it is reversible with proper preventive care, marginal gingivitis has a disturbingly high prevalence in children (Stratford, 1975). Complete edentulousness - total loss of teeth, a state indicating utter failure of past preventive and restorative treatment - has been reached by approximately 25 per cent of the adult population of England and Wales by the age of 40 and this figure is 75 per cent by the age of 60 (Gray et aL, 1970). There are indications that the situation now is improving and the results of a national survey conducted in 1978 are expected t o show less active disease, though the effects of past neglect will take several decades to work through the community. Nevertheless, these few figures serve to show the enormity of the problem. In the UK the amount of dental care delivered t o the community over the past 30 years, as measured by the number of courses of treatment delivered within the National Health Service has increased considerably. This has been achieved without dramatic increases in manpower (at present there are approximately 20 000 dentists, 1050 hygeinists and 500 auxiliaries in England and Wales), and with dentistry receiving a declining share of total NHS expenditure (at present 3.7 per cent though at one time dentistry had 10 per cent). The improvement in dental hLalth has, presumably, resulted from increasing efficiency within the profession. It is clear however that the gap between the need for care and the ability of the profession t o meet the need will never be closed by 99
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increased treatment efficiency alone. If this is true of societies in Western Europe and North America then it is clear that a system based on professional dentists providing sophisticated restorative treatment will be even less likely to meet the needs of the developing countries of the world where vast populations have virtually no access to dental care services. These arguments point to the need for increasing emphasis on prevention of oral disease as the best long-term solution. We now know enough about the causes and mechanism of dental caries and periodonial disease for both to be regarded as completely preventable diseases and this is illustrated by the families of many dentists and other highly motivated individuals who are free of disease. The immediate challenge lies not only in devising and perfecting new, more efficient and more readily applicable preventive measures but in learning how best t o apply known preventive measures to the community at large. Another sense in which the cliche that ‘prevention is better than cure’ is undoubtedly true is in the effect of disease on the individual. The need to restore carious teeth or to replace lost teeth obviously presents the individual with problems of time, discomfort, inconvenience and expense. Unless satisfactory prosthetic treatment is received tooth loss will result in aesthetic deterioration and impairment of speech and mastication. Though rarely of life-threatening significance this latter can be important in aged individuals and the impact on the quality of life of difficulty with chewing should not be underestimated. Loss of teeth leads inevitably to atrophy of the supporting alveolar bone which may be accelerated by the provision of inadequate dentures. Following tooth loss there is a progressive alteration in the whole of the facial skeleton and associated musculature and disease of oral soft tissues and of the ternperomandibular joint may supervene. The pain and distress caused by inflammation of the pulp, due to progression of caries, is all too familiar. As this condition is caused by bacteria, the possibility of spread of infection to surrounding bone, to and through contiguous soft tissues, and t o more distant sites via the blood stream and lymphatic system must constantly be borne in mind. In most parts of the world caries today rarely leads t o fatal infection but deaths can and do occur, particularly if the patient does not have access to surgical and, or, antibiotic treatment. A visit t o any dental emergency clinic will confirm the extent of personal suffering which arises from dental infections. Oral infections in patients with rheumatic or congenital heart disease are particularly dangerous because of the danger of provoking infective endocarditis. Aetiology of dental canes An over-simplified, but essentially accurate, concept of the aetiology and pathogenesis of dental caries has existed for the best part of a century and a half and has come to be known as the chemico-parasitic or acidogenic theory This holds that bacteria present in the mouth interact with retained food particles to produce substances capable of dissolving enamel. The three essential components of the caries process are thus immediately appreciated, namely the presence of a susceptible tooth, the presence of microorganisms, and dietary factors. An enormous amount of subsequent research has confirmed this concept and 100
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provided detail concerning those features of the structure and composition of teeth which affect their susceptibility to caries, detail on which bacteria are most likely to be involved, and detail on those components of the diet which are particularly dangerous. Many other factors, both local and systemic, influence the likelihood of caries developing and its speed of progression, so that caries is truly a multifactorial disease. As might be expected from such a highly complex situation, the caries process is dynamic, periods of attack alternating with periods of stasis, or with regression of the lesion. This fact has an important bearing on any clinical approach t o the management of patients, the prime objective of which should be to tip the balance towards arrest or regression - that is to control the cariogenicity of the patient’s mouth and to encourage repair of damaged tooth structure.
The essential role of bacteria The presence of bacterial plaque is essential to the production of a carious lesion; it is bacterial enzymes which produce acid from foodstuff and it is the structure, or consistency, of plaque which helps retain acid in contact with the tooth and which protects it from the diluting and buffering effect of saliva. Proof of the absolute necessity for bacteria first came from the experiments of Orland and collaborators (1955) who showed that, while susceptible rodents on a highly cariogenic diet did not develop caries under germ-free conditions, caries developed in the same animals when fed the same diet after the introduction of bacteria. Keyes (1960) established the infectious and transmissable nature of dental caries; he mono-infected germ-free animals with known strains of streptococci and showed that the organisms, and susceptibility to caries, became transferred to previously uninfected litter mates. Subsequently the use of gnotobiotic rodents (ie animals carrying a known flora) has done much t o sort out which species of bacteria, and which combination of species, are cariogenic to these animals and which might, therefore, be cariogenic t o man. These organisms, mostly streptococci of the viridans type, particularly the species known as Streptococcus mutans, and some strains of Lactobacilli and Actinomyces, are cariogenic in animals and man. Such organisms isolated from human lesions have been used to induce caries in previously caries-free monkeys maintained on diets rich in sucrose and other carbohydrates; the organisms, and hence susceptibility t o caries, can be transferred readily from mother to offspring, though adult cage mates, in whom the oral flora is already established, are more resistant. Organisms of this type are more numerous in the mouths of caries-active than of caries-inactive persons, and their distribution within the mouth to some extent mirrors the distribution of carious lesions. It thus seems possible to regard dental caries in man as an infectious and transmissable.disease, though there may be several different organisms involved. The familial pattern of canes prevalence partly may be explained by cross-infection between parents and children, though diet and other environmental factors are also important. The essential cariogenicity of these organisms lies in their ability to produce acid rapidly from carbohydrate, that is they are acidogenic, in their ability t o survive under acid conditions, that is they are aciduric, and in their propensity to adhere t o and proliferate 101
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upon hard tooth surfaces. Most cariogenic organisms also have the ability, through possession of the necessary enzyme systems, to synthesise large amounts of extracellular polysaccharide from dietary sugars. These polysaccharides, mostly polymers of glucose, (ie polyglucans of variable complexity) make up much o f the interbacterial matrix of dental plaque. Plaque polysaccharides are sticky, gelatinous substances which help bacteria adhere to the tooth, and which affect the permeability characteristics of the plaque, thus influencing the rate at which saliva can neutralise or dilute acid formed in the depths of the plaque, and slowing the diffusion away from the tooth of the products of mineral dissolution. It is clear that dental plaque is a very heterogenous structure which varies in composition from site t o site on any given tooth surface, from tooth to tooth, and from mouth to mouth. Not all portions of enamel covered by plaque become carious, indicating important regional variations in the pathogenicity of dental plaque.
Acid production by plaque microorganisms Following the ingestion of readily fermentable carbohydrate the pH within plaque can fall t o 4.5 or 5.0 within 1-3 minutes and it usually takes 10-30 minutes for this to approach neutrality again; this produces a characteristic graphknown as a ‘Stephan curve’ after the Swedish dental scientist who first brought it into prominence (Stephan, 1944). Many studies of this type have been conducted, using antimony electrodes inserted into plaque or, more recently using indwelling electrodes in partial dentures with recordings made by telemetry (Imfeld, Hirsch & Muhllemann, 1978). These have shown that the pH falls in individuals with high caries activity are both more profound and more sustained than in individuals with low caries activity, partly because of greater plaque thickness in the former and, possibly, also because their mouths have a greater population of cariogenic bacteria. Furthermore, it is well recognised that second and subsequent intakes of carbohydrate, delivered before the plaque pH has re-stabilised, depress pH even further producing a ‘staircase effect’. Such levels of acidity are dangerous because, whereas at neutrality human saliva and plaque fluid are supersaturated with calcium and phosphate, at about pH 5 this saturation is overcome and enamel solubility increases markedly. Not surprisingly, low-molecular-weight carbohydrates produce the most rapid and significant pH falls because they most readily diffuse into the depths of plaque. In practical dietary terms it is sugars like sucrose, glucose and fructose which are most important in this regard. The acids involved can be identified, for example by gas liquid chromatography, in sugar-saliva mixtures, or after incubation of foodstuffs with saliva or plaque microorganisms and, with more difficulty, in dental plaque and carious enamel itself. There are many glycolytic bacteria in plaque and these include both homolactate fermenters and heterolactate fermenters. Lactate, acetate, propionate and other aliphatic acids are produced; but, of these, lactate is the most important both because it is produced in the largest quantities and because it is the strongest of these acids. It has been estimated (R.A.D. Williams, personal communication) that, if 50 per cent of bacteria in plaque are glycolytic, each milligram of plaque produces 102
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its own weight of lactic acid whilst growing to that weight on a carbohydrate substrate. A mouth may grow 10 mg of plaque per day but most of this acid is harmlessly diluted in saliva: it only requires a small percentage, however, if retained within the plaque, to produce a decalcifying pH. I have mentioned the importance of regional variation in plaque microflora. One such variation which has attracted attention is the presence of Veillonellae and the symbiotic relation between this species and several strains of streptococci. Veillonellae lack certain key enzymes of glycolysis and of the pentosephosphate pathway. They are, however, able to grow well in the presence of streptococci where they utilise the lactate produced by these organisms, generating propionic and acetic acids in the process. These latter acids are, fortunately, less strong than lactate, so that such mixed cultures result in less acid formation. Other acids are produced from protein catabolism by, for example, Bacteroides, but these make a minor contribution. Base is also produced, by decarboxylation of amino acids and hydrolysis of urea, so that alkaline conditions can exist in plaque and these circumstances favour its mineralisation to produce dental calculus. In general, however, nett acid production by plaque in stagnation areas utilising carbohydrate substrates is more usual.
The role of dietary carbohydrate: sucrose the ‘arch criminal’ The relative cariogenicity of different carbohydrates depends on frequency of intake, on their physical form - sticky, retentive substances such as toffee being worst - and on their chemical type. Complex carbohydrates such as starch are not digested to any significant degree in the mouth. Low-molecular-weight substances, particularly sugars, are more dangerous because they can more readily diffuse into the plaque and are more rapidly metabolised by the bacteria. Sucrose has been described as the ‘arch criminal’ of dental caries (Newbrun, 1967). It is much more cariogenic than glucose, for example, which diffuses just as readily into plaque and produces acid just as quickly. Sucrose is the most frequently consumed sugar in modern diets and some explanation of the mechanism by which it produces damage is now available. Cariogenic microorganisms synthesize extracellular polysaccharides faster from this disaccharide than from any other sugar; faster even than from equivalent mixtures of its constituents glucose and fructose. The energy liberated from rupture of the disaccharide bond is used, with the aid of bacterial glucosyl transferases, to synthesize complex polyglucans from the glucose. Fructose is synthesized to polyfructans of the levan type which are not so stable and may be converted to acid quite quickly. Plaque bacteria also make, and store, intracellular polysaccharides of the glycogen type from dietary sugars. Both intracellular and extracellular polysaccharides may be used as substrates for acid production in periods when n o food is being taken into the mouth. It is as important, therefore, to remove the bacteria as to restrict carbohydrate intake, and teeth might well be cleaned before meals with as much effect as after meals; indeed all our knowledge of the pathogenesis of caries points t o before-meal cleaning as the most rational oral hygiene approach to caries prevention. A number of studies have shown that the presence of sucrose in the diet favours the implantation of cariogenic streptococci into the mouths of rats, hamsters, monkey and man (eg, Huxley, 1974). 103
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Epidemiological evidence on the relation between diet and dental caries Several studies are frequently quoted under this heading for they have become classical pieces of evidence that diet has a profound influence on caries activity. In the 1930s the inhabitants of the isolated South Atlantic island of Tristan da Cunha lived on a diet of local vegetables, meat and fish and had excellent dental health. Increasing importation of manufactured foods in the intervening years led to increasing caries and finally, with the evacuation of the islanders to Britain, to marked caries incidence (Fisher, 1972). Caries incidence figures in children of several European countries during the second World War were significantly depressed in parallel with the reduced sugar consumption of that time. Once sweets were no longer rationed caries rapidly increased (Marthaler, 1967). Two longitudinal studies on institutionalised individuals have also become classics. The first of these is the Vipeholm study in which various groups of adults in a mental hospital were allowed access to table sugar and toffees in different amounts and at various frequencies. They had previously been shown, over a period of several years, t o have low caries on a nutritionally adequate diet low in carbohydrate. Caries increased significantly .when sucrose-containing foods were made available, particularly in those who consumed sucrose bet ween meals; sucrose confined to meal-times was far less dangerous. Furthermore, toffees which adhered t o the teeth and maintained high sucrose levels in saliva for prolonged periods were far more damaging than those which were rapidly 1954). cleared from the mouth (Gustaffson et d., The second is a study of 80 children raised at Hopewood House, New South Wales, Australia, on a vegetarian/dairy-product diet excluding refined carbohydrates. In spite of poor oral hygiene and low levels of fluoride in the water supply children in the 5-13 year age group had only about 10 per cent of the caries level of the general population. After leaving the home these same children rapidly developed caries, indicating that the caries protection was not a nutritional effect during tooth development (Harris, 1963). Individuals suffering from hereditary fructose intolerance provide another good example of the cariogenicity of sucrose and the relatively low cariogenicity of other carbohydrates. If children with this inborn error of metabolism are to survive they must avoid foods containing fructose and sucrose, though they can and do consume milk sugar (lactose) and starch. Such individuals have remarkably little - indeed often zero - caries (Linden & Nisell, 1964; Newbrun, 1967; Hess & Graf, 1975). A number of the above studies have recently been criticised by Jackson (1978); but, although he raises many valid qualifications, they do not detract from the overwheming weight of evidence that sugar causes caries. In addition to these observations on man there is a large literature o n the relative cariogenicity of different foodstuffs in animals, mostly rodents (see, for example Stephan, 1966; Bibby, 1975; Grenby, 1976). In general these confirm the importance of sucrose content, of physical texture and adhesiveness, and of the molecular weight of sugar polymers. It should be remembered that most fruits contain fermentable sugars and are therefore moderately cariogenic. This includes apples, which are ineffective in cleaning the teeth because they do 104
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not remove plaque (Marthaler, 1968: Longhurst & Berman, 1973); it is time this popular misconception was dispelled. This does not mean, however, that apple eating should be discouraged as apples are infinitely preferable snacks t o sucrosecontaining foods. Furthermore they promote salivary flow which must be beneficial. Nutritional factors of importance in resistance of the teeth to dental caries Systemic nutritional factors, as opposed t o local dietary Pactors which influence dental caries, operate at two levels; first, during the period of tooth formation, exerting their effects via the composition and structure of the teeth; secondly, throughout life by influencing the composition and flow of saliva. There is no doubt that the poor nutrition common in many of the world’s preindustrialised societies results in a relatively high prevalence of hypoplastic and hypomineralised defects in teeth (eg Infante & Gillespie, 1974; Enwonwu, 1978). For many years such teeth were thought t o be no more susceptible to caries than normal, or even to be caries resistant. It now appears that this was an erroneous impression, created by the low caries activity in these communities who did not eat cariogenic diets. Indeed recent work in Guatemala (Infante & Gillespie, 1977) shows that children with linear hypoplasia of anterior deciduous teeth had a significantly greater amount of caries in the apparently normal posterior dentition than did their peers who did not show hypoplastic defects. This suggests that the synergistic effect of undernutrition and infection, thought to be responsible for the enamel hypoplasia in the anterior teeth, predisposes clinically normal-looking posterior teeth to caries. Furthermore there are many reports of severely dysplastic teeth becoming seriously destroyed by caries (Sweeney, Saffir 8c de Leon, 1971), such misleading terms as ‘melanodontia’ (Mayer & Baume, 1966) or ‘odontoclasia’ (Jones, Larson & Prichard, 1930) having been applied t o this appearance in the past. The only nutritional factor of proven importance in influencing the canes resistance of teeth during their formation is fluoride. This acts partly by altering the shape of teeth, making them slightly smaller, with less plaque-retentive fissures and partly by making the hydroxy apatite crystals of enamel less soluble in organic acids by incorporation of F ions into the lattice (Levine, 1976; Murray, 1976). Other trace elements with a less marked effect are molybdenum and possibly also strontium, vanadium, lithium and boron (Navia, 1970; Curzon & Losee, 1977). Trace element effects apart, surprisingly little is known of what constitutes a ‘caries-resistant tooth’ (Ciba Symposium, 1965). It is probable that, in Western communities at least, intrinsic differences in susceptibility are swamped by the microbial/dietary/salivary interactions at the tooth surface. Finally, the nutritional quality of food must influence the function of salivary glands and thus the quality and flow rate of saliva (Dawes, 1970). Saliva is a highly important factor in the pathogenesis of caries and in oral defence mechanisms. Afiart from the diluting and washing effect saliva contains buffers; antibacterial factors like lysozyme and lactoperoxidase (Mandel, 1976); calcium, phosphorus, fluoride and other ions which inhibit tooth demineralisation; IgA 105
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which modifies bacterial colonisation of the tooth surface (Brandtzaeg, 1976); glycoproteins which contribute to pellicle and plaque formation (Bowen, 1976). Little is known, however, of how nutritional factors mediated via saliva influence caries activity. Relation between diet, nutrition and periodontal disease Because gingivitis and periodontitis represent an interaction between irritants derived from dental plaque and the host tissue response, nutritional effects on systemic health must be considered in conjunction with local dietary effects on plaque formation and bacterial metabolism. Severe protein-energy malnutrition and vitamin deficiencies certainly reduce the r’esistance of periodontal tissues to infection. Amongst the latter vitamin A, because of its importance to epithelial integrity, and vitamin C, because of its importance in collagen metabolism, are pahicularly important. It is not surprising, therefore, that conditions like acute necrotising ulcerative .gingivitis are more common in malnourished children of the low socio-economic groups in developing countries (eg, Enwonwu, 1978). Nonetheless, epidemiological surveys in many parts of the world have shown no significant correlation between nutritional status, as determined by biochemical tests, and the general level of periodontal disease (Russell, 1963); the relation between plaque volume and disease seems t o be dominant (Ramfjord, Kerr & Ash, 1966). Nevertheless, as Navia (1977) has argued, such studies have usually been made on advanced disease and nutritional effects on the all-important initial stages have been little studied. Furthermore the biochemical estimations of nutritional status are often single assessments made once disease is established and these tell us little of the situation during the initiation and progression of disease. Repair processes in periodontal tissues are bound to be influenced by nutrition, as is the host’s immune response to plaque antigens (see Susskind, 1977). The ecology of gingival plaque must be influenced partly by local dietary effects (Loesche, 1968) but until our knowledge of which organisms are important in the pathogenesis of periodontal disease improves, little can be concluded. Egelberg (1965) has shown that dogs on a hard diet containing large amounts of gristle have less plaque and less periodontal disease than those on softer diets of the same compositions but minced; it is doubtful if such large differences in texture apply to modern man. We have already seen that the occasional apple and carrot is ineffective in promoting an improvement in gingival health. The frequent intake of refined carbohydrate certainly promotes plaque formation in all the usual sites on the tooth surface, and thus promotes caries. Cariogenic diets are thus bound to promote periodontal disease also, but the association has not been closely investigated in man. The prevention of dental caries and periodontal disease From the above outline of the aetiology and pathogenesis of dental caries it is evident that attempts to break the complex sequence of events leading to disease can be directed at: 1. Dietary control (see below) 2. Plaque control : this includes a range of mechanical, chemical and immuno106
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logical methods for the removal of established plaque and the prevention of plaque growth. 3. Increasing the resistance of the tooth: this includes adequate nutrition during tooth formation, particularly the intake of optimum amounts of fluoride, the application of topical fluorides and remineralising solutions, and fissure sealants. Many of these methods will also help in the control of periodontal disease.
Theoretical approaches to the dietary control o f dental caries Space does not permit a detailed review of the literature concerned with dietary control of caries, though several aspects are covered in the subsequent papers. It is important t o ensure nutritional adequacy during growth and development of the teeth, and throughout life, so that salivary function and other body defences are maintained at optimal levels. Once the teeth have erupted we can attempt to break the chain of diet-related events leading to caries by: (1) Reducing the amount and frequency of intake of cariogenic carbohydrates; (2) modification of the form and texture of potentially cariogenic foods; (3) encouraging consumption of protective natural foods; (4) replacing sucrose in the diet with less cariogenic sweeteners; (5) adding cariesinhibitory substances to food. (1,2) : Controlling cariogenic foods. Measures here involve the restriction of sucrose to meal times, avoidance of adhesive fermentable carbohydrates, the limitation of between-meal snacks and the replacement of biscuits and the like with nuts, cheese, celery or apples. A valuable study of the effect on plaque pH of a range of British snack foods has recently been presented by Rugg-Gunn, Edgar & Jenkins (1978). (3): Protective natural foods. Animal experiments have shown that oat husks, wheat germ, raw molasses and chocolate contain protective factors. However, if man consumes these substances he does so in association with sucrose so that there is no beneficial effect. Dairy products, notably milk (McDougall, 1977) and cheese, are protective. This has considerable practical importance with respect t o meal patterns. For example if a cheese course is taken, in the French manner, before a sweet course, the pH fall in plaque as a result of the sweet is substantially reduced (Rugg-Gunn et at., 1975). Nuts o r a little cheese after a meal promote salivation which also reduces the pH drop (Geddes et al., 1977). (4): Sucrose substitutes. A substantial number of sucrose substitutes has been investigated and several have been commercially exploited (Newbrun, 19 73). These include cyclamates, saccharin, aspartame, sorbitol and xylitol. Most of these are inherently much sweeter than sucrose and can be used in small quantities. Nevertheless several are under suspicion as carcinogens, though in doses far in excess of those normally consumed by man. A further limitation is that most are vastly more expensive t o produce than sucrose. The agent attracting most current interest is xylitol, which has received extensive animal and human trials, particularly in Finland (Scheinin & Makinen, 1975; Makinen, 1978). 107
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(5): Food additives. Phosphate additives are thought to work on the principle of saturating plaque fluid with phosphate ions, inhibiting enamel demineralisation and favouring remineralisation by a mass action effect, and preventing depletion of plaque phosphate by the micro organisms during growth. Unfortunately the promise of animal experiments has not been borne out in man. Of the inorganic phosphates trimetaphosphate is apparently more effective than ortho-phosphate or pyro-phosphate (Harris, 1970a, b ) . Organic phosphates which have been studied include phytate, 0-glycerophosphate (Grenby & Bull, 1978) and calcium-sucrose-phosphate. The latter, under the trade name ‘Anticay’ has undergone extensive clinical trials in Australia but these are difficult to evaluate because some of the preparations also contained significant amounts of fluoride (Harris et aL, 1969). Finally fluoride may be delivered in foods, milk and table salt being the most commonly used vehicles. They are not as effective as water fluoridation but form a valuable alternative in communities resistant to the latter (see review by Murray, 1976). Bibliop a p hy More detailed coverage of many of the topics mentioned, together with fuller references, can be found in : Nizel, A.E. (1968) : The science of nutrition and its application in clinical dentistry. Philadelphia: Saunders. Caldwell, R.C. & Stallard, R.E. (1 977): A textbook of preventive dentistry. Philadelphia: Saunders. Jenkins, G.N. (1978): The physiology and biochemistry of the mouth, 4th edn. Oxford: Blackwell. Silverstone, L.M., Johnson, N.W., Hardie, J.M. & Williams, R.A.D. (1978): Dental caries: aetiology, pathology and prevention. London: MacMillan Press. Andlaw, RJ. (1977): Diet and dental caries - a review. J. Hum. Nutr. 31, 45-52. Levine, R.S. (1977): The aetiology of dental caries - an outline of current thought. Znt. Dent. J. 27, 341-348 Winter, G.B. (1976): Maternal nutritional requirements in relation to the subsequent development of teeth in children. J. Hum. Nutr. 31, 93-99
References Bibby, B.G. (1975): The cariogenicity of snack foods and confections. J. Am. Dent. Ass. 90, 121-132. Bowen, W.H. (1976): Nature of plaque. Oral Sci. Rev. 9, 3-21. Brandtzaeg, P. (1976): Synthesis and secretion of secretory immunoglobulins with special reference to dental caries. J. Dent. Res. 55, Special Issue C, 102-114. Ciba Foundation Symposium (1965): Caries resistant teeth. London: J. & A. Churchill. Cowley, G. & MacPhee, T. (1975): Essentials of periodontology and periodontics, 2nd edn. Oxford: Blackwell Scientific. Curzon, M.E.J. & Losee, F.L. (1977): Dental caries and trace element composition of whole human enamel. Eastern United States.J. A m . Dent. Ass. 94, 1146-1150. Dawes, C. (1970): Effects of diet on salivary secretion and composition. J. Dent. Res. 49, 1263-127 2. Egelberg, J. (1965): Local effects of diet on plaque formation and development of gingivitis in dogs. Odont. Revy 16, 31-60.
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Enwonwu, C. (1978): Interface of nutrition and dentistry in pre-industrialised tropical countries. Trop. Dent. J. 1, 19-44. Fisher, F.J. (1972): The pattern of dental caries in Trista da Cunha. DentalPractitioner 22, 267-270. Geddes, D.A.M., Edgar,W.M., Jenkins, G.N. & Rugg-Gunn, A.J. (1977): Apples, salted peanuts and plaque. Br. Dent. J. 142, 317-319 Gray, P.G., Todd, J.E., Slack, G.L. & Bulman, J.S. (1970): Adult dental health in England and Wales in 1968. London: Her Majesty’s Stationery Office. Grenby, T.H. (1976): Manufactured foods and dental decay. Nutr. Fd Sci. 45, 6-10. Grenby, T.H. & Bull, J.M. (1978): Dental caries in laboratory rats from breakfast cereals and its control by a calcium glycerophosphate additive. Archs Oral Biol. 23, 675-680. Gustafsson, B.E., Quesnel, C.E., Lanke, L.S., Lundqvist, C., Grahnen, H., Bonow, B.E. & Krasse, B. (1954): The Vipeholm dental caries study. The effect of different levels of carbohydrate intake on caries activity in 436 individuals observed for 5 years. Acta Odont. Scand. 11, 232-364. Harris, R. (1963): Biology of the children of HopewoodHouse, Bowral, Australia 4. Observations of dental caries experience extending over 5 years (1957-1961).J. Dent. Res. 42, 1387-1398 a r r i s , R., Schamschula, R.G., Beveridge, J. & Gregory, G. (1969): Calcium sucrose phosphate as a cariostatic agent in children aged 5-17 years: part IV. Aust. Dent. J. 42-49 Harris, R.S. (1970a):Fortification of foods and feed-products with anti-caries agents. J. Dent. Res. 49, 1340-44. Harris, R.S. (19706): Minerals: calcium and phosphates. I n Dietary chemicals us. dental caries, R.F. Gould (Ed). Amer. Chem. SOC:Advances in Science Series 94, 116-122 Hess, J. & Graf, H. (1975): Zahnplaque-pH bei Patienten mit hereditaren Fruktose-Intoleranz. Schweiz. Mschr. Zahnheilk. 85, 141-153. Huxley, H.G. (1974): The effect of dietary carbohydrate upon colonisation of plaque b y Streptococcus mutans in rats. Archs Oral Biol. 19, 941-946. [mfeld, Th., Hirsch, R.S. & Muhlemann, H.R. (1978): Telemetric recordings of interdental plaque pH during different meal patterns. Br. Dent. J. 144,40-45. [nfante, P.F., Gillespie, G.M. (1974): An epidemiological study of linear enamel hypoplasia of deciduous anterior teeth in Guatemalan children. Archs Oral BioL 19, 1055-1061. [nfante, P.F., Gillespie, R.M. (1977): Enamel hypoplasia in relation to caries in Guatemalan children. J. Dent. Res. 56, 493-498. Jackson, D. (1978): Sugar and dental caries: myth and fact. The Probe 19, 388-394. Jones, M.R., Larson, N.P. & Prichard, G.P. (1930): Dental disease in Hawaii - I: odontoclasia: a clinically unrecognised form of tooth decay in the pre-school child of Honolulu. Dent. Cosmos 72, 439-450. Keyes, P.H. (1960): The infectious and transmissable nature of experimental dental caries. Archs Oral Biol. 1, 304-326. Levine, R.S. (1976): The action of fluoride in caries prevention. A review of current concepts. Br. Dent. J. 140, 9-14. Linden, L. & Nisell, J. (1964): Hereditary intolerance to fructose. SvenskLakartidn. 61, 3185. Loesche, W.J. (1968): Importance of nutrition in gingival crevice microbial ecology. Periodontics 6, 245-249. Longhurst, P.L. & Berman, D.S. (1973): Apples and gingival health. Report of a feasibility study. Br. Dent. J. 134, 475-479. McDougall, W.A. (1977): Effect of milk on enamel demineralisation and remineralisation in vitro. Caries Res. 11, 166-172. Makinen, K.K. (1978): Biochemical principles of the use of xylitol in medicine and nutrition with special consideration of dental aspects. Experientia, Suppl. 30, in press. Mandel, I.D. (1976): Non-immunologic aspects of caries resistance. J. Dent. Res. 55, Special Issue C. 22-C31. Marthaler, T. (1967): Epidemiological and clinical dental findings in relation to intakes of carbohydrates. Caries Res. 1, 222-238. Marthaler, T. (1968): Apfel, Gesundheit und Kauorgan. Schweiz. Mschr Zahnhlk 78, 823-836. Mayer, J. & Baume, L.J. (1966): Pathologie de la melandontie infantile, de l’odontoclasie et de la carie circulaire. Rev. Suisse Odontol. 76, 48-92. 109
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Murray, J.J. (1976): Fluorides in caries prevention. In Dentalpractitioner handbook, No. 20. Bristol: Wright. Navia, J.M. (1970): Effects of minerals on dental caries. I n Dietary chemicals us dental caries. Am. Chem. SOC:Advances in Science Series No. 94. Navia, J.M. (1977): Nutrition and oral disease. In A textbook of preventive dentistry, ed Caldwell, R.C. & Stallard, R.E. Philadelphia: Saunders. Newbrun, E. (1967): Sucrose, the arch criminal of dental caries. Odont. Rev. 18, 373-386. Newbrun, E. (1973): Sugar, sugar substitutes and non-caloric sweetening agents. Int. Dent. J. 23, 328-345. Orland, F.J., Blayney, J.R., Harrison, R.W., Reyniers, J.A., Trexler, P.C., Ervin, R.F., Gordon, H.A. & Wagner, M. (1955): Experimental caries in germ-free rats inoculated with enterococci. J. A m . Dent. Ass. 50, 259-272. Pelton, W.J., Pennel, E. & Druzina, A. (1954): Tooth mortality experience of adults. J. A m . Dent. Ass. 49, 439. Ramfjord, S.P., Kerr, D.A. & Ash, M.M. (1966):.World workshop in periodontics.lJniv. of Michigan, Ann Arbor, Michigan. Rugg-Gunn, A.J., Edgar, W.M., Geddes, D.A.M. &Jenkins, G.N. (1975): The effect of different meal patterns upon plaque pH in human subjects. Br. Dent. J. 139, 351-356. Rugg-Gunn, A.J., Edgar, W.M. & Jenkins, G.N. (1978): The effect of eating some British snacks upon the pH of human dental plaque. Br. Dent. J. 145, 95-100. Russell, A.L. (1 963): International nutrition surveys: a summary of preliminary dental findings. J. Dent. Res. 42, 233-244. Scheinin, A. & Makinen, K.K. (1975): Turku sugar studies I-XXI. Final report on the effect of sucrose, fructose and xylitol diets on the caries incidence in man. Acta Odont. Scand. 33, Suppl. 70. Schluger, S., Yuodalis, R.A. & Page, R.C. (1977): Periodontal disease. Philadelphia: Lea & Febiger. Stallard, R.E. (1967): Current concepts of periodontal disease. J. Dent. Child. 34,204-210. Stephan, R.M. (1 944): Intraoral hydrogen ion concentrations associated with dental caries activity. J. Dent. Res. 23, 257-266. Stephan, R.M. (1966): Effect of different types of human foods on dental health in experimental animals. J. Dent. Res. 45, 1551-1561. Stratford, J.M. (1975): Gingivitis in school-age children: a review of the literature. J. Irish Dent. Ass, 21, 7-14. Susskind, R.M. Editor (1977): Malnutrition and the immune response. New York: Raven Press. Sweeney, E.A., Saffii, A.J. & de Leon, R. (1971): Linear hypoplasia of deciduous incisor teeth in malnourished children. A m . J. Clin. Nutr. 24, 29-31. Todd, J.E. (1975): Children’s dental health in England and Wales 1973. Office of Population. Censuses and Surveys. London: HMSO.
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1: Aetiology of dental disease and theoretical aspects of dietary control
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N. W. JOHNSON, MDSc, PhD, FDS, FRACDS, MRCPath Department of Oral Pathology, The London Hospital Medical College, Turner Street, London E 1 2AD, England. The term ‘dental disease’ should be taken to include both dental caries and periodontal disease for both are almost universally prevalent, both result in substantial tooth loss and both have a common cause, namely dental plaque. Because this symposium is concerned with dental disease in children it is inevitable that our discussion will be dominated by caries. This is because caries activity is highest in childhood and adolescence and it is not normally until adulthood that periodontal disease has advanced sufficiently to become a significant cause of discomfort to the patient or a major cause of tooth loss. Nevertheless both disease processes commence early in life and patterns of diet and oral hygiene, which so strongly influence the rate of progress of disease, are established at this time. Definition of dental caries Dental caries is a form of progressive destruction of enamel, dentine and cementum initiated by microbial activity at the tooth surface. In short, certain types of bacteria preferentially colonise certain sites on the tooth surface which are protected from the natural cleansing movements of the lips, cheeks and tongue and accumulate to form dental plaque. These bacteria metabolise dietary constituents, notably carbohydrate and sucrose in particular, to form organic acids. The acids are held close to the tooth surface by the relative impermeability of the plaque and are thus protected from the diluting and buffering affects of saliva. The acids so formed have an opportunity to dissolve tooth substance and this occurs slowly, intermittently, and in depth. Destruction of tissue is characteristically preceded by softening, brought about by partial dissolution of mineral ahead of the final destruction of the organic matrix of the tissue and residual mineral. Because of the characteristic pattern of alteration in depth, caries can be distinguished from other destructive processes of the crowns of the teeth such as abrasion due to mechanical wear and erosion due t o strongly acidic fluids which remove completely thin layers of the surface. Definition of periodontal disease Though there are specific forms of periodontal disease associated with specific infections and with certain systemic diseases which depress the host defence mechanisms, the unqualified term ‘periodontal disease’ refers to the presence of progressive, destructive inflammatory lesions of the tissues surrounding the teeth. These lesions are also initiated by the presence of dental plaque, residing on the tooth surface in contact with gingival soft tissue. The tissues are damaged by the direct effect of toxins and enzymes liberated by plaque microorganisms. These agents diffuse into the tissues where they also provoke inflammation. 98
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Furthermore, many plaque products, such as the lipopolysaccharide endotoxins of Gram-negative bacteria and the lipoteichoic acids of Gram-positive bacteria are antigenic, so that immunological reactions are provoked in the tissue. The immune inflammatory response, if sustained over a substantial period of time due to the continued presence of plaque, itself results in tissue damage; this is mediated by lytic enzymes released from polymorphs and macrophages and by hypersensitivity reactions of both the humoral and cell-mediated types (Cowley & MacPhee, 1975; Schluger, Yuodalis & Page, 1977). The earliest sign of periodontal disease is marginal gingivitis, ie inflammation of the gum margins. This stage of the disease is reversible, but once destruction has extended into the periodontal ligament which attaches the tooth root t o the surrounding bone, some permanent loss of tooth support is inevitable. The problem of dental disease Dental caries and periodontal disease are the most common diseases affecting Western man, with a prevalence of almost 100 per cent. In England and Wales a national survey of adults conducted in 1968 found only three people in 1000 with 28 or more teeth present and free from caries. In Britain 25 per cent of all teeth erupted in children up t o 1 2 years of age have been affected by caries; by the age of 15 this has risen to 33 per cent and by age 30, to 67 per cent. The Survey of Children’s Dental Health in England & Wales 1973 (Todd et aZ., 1975) revealed a total number of decayed, missing and filled teeth of 3.9 at age six, 5.0 at age eight and 8.4 at age 15. Many workers believe that destructive periodontal disease begins in childhood, but that it may not be recognised until the third decade, after irreversible changes have occurred (Stallard, 1967). Certainly after the age of 35 Periodontal disease becomes the major cause of tooth loss (Pelton, Pennel & Druzina, 1954). Though it is reversible with proper preventive care, marginal gingivitis has a disturbingly high prevalence in children (Stratford, 1975). Complete edentulousness - total loss of teeth, a state indicating utter failure of past preventive and restorative treatment - has been reached by approximately 25 per cent of the adult population of England and Wales by the age of 40 and this figure is 75 per cent by the age of 60 (Gray et aL, 1970). There are indications that the situation now is improving and the results of a national survey conducted in 1978 are expected t o show less active disease, though the effects of past neglect will take several decades to work through the community. Nevertheless, these few figures serve to show the enormity of the problem. In the UK the amount of dental care delivered t o the community over the past 30 years, as measured by the number of courses of treatment delivered within the National Health Service has increased considerably. This has been achieved without dramatic increases in manpower (at present there are approximately 20 000 dentists, 1050 hygeinists and 500 auxiliaries in England and Wales), and with dentistry receiving a declining share of total NHS expenditure (at present 3.7 per cent though at one time dentistry had 10 per cent). The improvement in dental hLalth has, presumably, resulted from increasing efficiency within the profession. It is clear however that the gap between the need for care and the ability of the profession t o meet the need will never be closed by 99
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increased treatment efficiency alone. If this is true of societies in Western Europe and North America then it is clear that a system based on professional dentists providing sophisticated restorative treatment will be even less likely to meet the needs of the developing countries of the world where vast populations have virtually no access to dental care services. These arguments point to the need for increasing emphasis on prevention of oral disease as the best long-term solution. We now know enough about the causes and mechanism of dental caries and periodonial disease for both to be regarded as completely preventable diseases and this is illustrated by the families of many dentists and other highly motivated individuals who are free of disease. The immediate challenge lies not only in devising and perfecting new, more efficient and more readily applicable preventive measures but in learning how best t o apply known preventive measures to the community at large. Another sense in which the cliche that ‘prevention is better than cure’ is undoubtedly true is in the effect of disease on the individual. The need to restore carious teeth or to replace lost teeth obviously presents the individual with problems of time, discomfort, inconvenience and expense. Unless satisfactory prosthetic treatment is received tooth loss will result in aesthetic deterioration and impairment of speech and mastication. Though rarely of life-threatening significance this latter can be important in aged individuals and the impact on the quality of life of difficulty with chewing should not be underestimated. Loss of teeth leads inevitably to atrophy of the supporting alveolar bone which may be accelerated by the provision of inadequate dentures. Following tooth loss there is a progressive alteration in the whole of the facial skeleton and associated musculature and disease of oral soft tissues and of the ternperomandibular joint may supervene. The pain and distress caused by inflammation of the pulp, due to progression of caries, is all too familiar. As this condition is caused by bacteria, the possibility of spread of infection to surrounding bone, to and through contiguous soft tissues, and t o more distant sites via the blood stream and lymphatic system must constantly be borne in mind. In most parts of the world caries today rarely leads t o fatal infection but deaths can and do occur, particularly if the patient does not have access to surgical and, or, antibiotic treatment. A visit t o any dental emergency clinic will confirm the extent of personal suffering which arises from dental infections. Oral infections in patients with rheumatic or congenital heart disease are particularly dangerous because of the danger of provoking infective endocarditis. Aetiology of dental canes An over-simplified, but essentially accurate, concept of the aetiology and pathogenesis of dental caries has existed for the best part of a century and a half and has come to be known as the chemico-parasitic or acidogenic theory This holds that bacteria present in the mouth interact with retained food particles to produce substances capable of dissolving enamel. The three essential components of the caries process are thus immediately appreciated, namely the presence of a susceptible tooth, the presence of microorganisms, and dietary factors. An enormous amount of subsequent research has confirmed this concept and 100
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provided detail concerning those features of the structure and composition of teeth which affect their susceptibility to caries, detail on which bacteria are most likely to be involved, and detail on those components of the diet which are particularly dangerous. Many other factors, both local and systemic, influence the likelihood of caries developing and its speed of progression, so that caries is truly a multifactorial disease. As might be expected from such a highly complex situation, the caries process is dynamic, periods of attack alternating with periods of stasis, or with regression of the lesion. This fact has an important bearing on any clinical approach t o the management of patients, the prime objective of which should be to tip the balance towards arrest or regression - that is to control the cariogenicity of the patient’s mouth and to encourage repair of damaged tooth structure.
The essential role of bacteria The presence of bacterial plaque is essential to the production of a carious lesion; it is bacterial enzymes which produce acid from foodstuff and it is the structure, or consistency, of plaque which helps retain acid in contact with the tooth and which protects it from the diluting and buffering effect of saliva. Proof of the absolute necessity for bacteria first came from the experiments of Orland and collaborators (1955) who showed that, while susceptible rodents on a highly cariogenic diet did not develop caries under germ-free conditions, caries developed in the same animals when fed the same diet after the introduction of bacteria. Keyes (1960) established the infectious and transmissable nature of dental caries; he mono-infected germ-free animals with known strains of streptococci and showed that the organisms, and susceptibility to caries, became transferred to previously uninfected litter mates. Subsequently the use of gnotobiotic rodents (ie animals carrying a known flora) has done much t o sort out which species of bacteria, and which combination of species, are cariogenic to these animals and which might, therefore, be cariogenic t o man. These organisms, mostly streptococci of the viridans type, particularly the species known as Streptococcus mutans, and some strains of Lactobacilli and Actinomyces, are cariogenic in animals and man. Such organisms isolated from human lesions have been used to induce caries in previously caries-free monkeys maintained on diets rich in sucrose and other carbohydrates; the organisms, and hence susceptibility t o caries, can be transferred readily from mother to offspring, though adult cage mates, in whom the oral flora is already established, are more resistant. Organisms of this type are more numerous in the mouths of caries-active than of caries-inactive persons, and their distribution within the mouth to some extent mirrors the distribution of carious lesions. It thus seems possible to regard dental caries in man as an infectious and transmissable.disease, though there may be several different organisms involved. The familial pattern of canes prevalence partly may be explained by cross-infection between parents and children, though diet and other environmental factors are also important. The essential cariogenicity of these organisms lies in their ability to produce acid rapidly from carbohydrate, that is they are acidogenic, in their ability t o survive under acid conditions, that is they are aciduric, and in their propensity to adhere t o and proliferate 101
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upon hard tooth surfaces. Most cariogenic organisms also have the ability, through possession of the necessary enzyme systems, to synthesise large amounts of extracellular polysaccharide from dietary sugars. These polysaccharides, mostly polymers of glucose, (ie polyglucans of variable complexity) make up much o f the interbacterial matrix of dental plaque. Plaque polysaccharides are sticky, gelatinous substances which help bacteria adhere to the tooth, and which affect the permeability characteristics of the plaque, thus influencing the rate at which saliva can neutralise or dilute acid formed in the depths of the plaque, and slowing the diffusion away from the tooth of the products of mineral dissolution. It is clear that dental plaque is a very heterogenous structure which varies in composition from site t o site on any given tooth surface, from tooth to tooth, and from mouth to mouth. Not all portions of enamel covered by plaque become carious, indicating important regional variations in the pathogenicity of dental plaque.
Acid production by plaque microorganisms Following the ingestion of readily fermentable carbohydrate the pH within plaque can fall t o 4.5 or 5.0 within 1-3 minutes and it usually takes 10-30 minutes for this to approach neutrality again; this produces a characteristic graphknown as a ‘Stephan curve’ after the Swedish dental scientist who first brought it into prominence (Stephan, 1944). Many studies of this type have been conducted, using antimony electrodes inserted into plaque or, more recently using indwelling electrodes in partial dentures with recordings made by telemetry (Imfeld, Hirsch & Muhllemann, 1978). These have shown that the pH falls in individuals with high caries activity are both more profound and more sustained than in individuals with low caries activity, partly because of greater plaque thickness in the former and, possibly, also because their mouths have a greater population of cariogenic bacteria. Furthermore, it is well recognised that second and subsequent intakes of carbohydrate, delivered before the plaque pH has re-stabilised, depress pH even further producing a ‘staircase effect’. Such levels of acidity are dangerous because, whereas at neutrality human saliva and plaque fluid are supersaturated with calcium and phosphate, at about pH 5 this saturation is overcome and enamel solubility increases markedly. Not surprisingly, low-molecular-weight carbohydrates produce the most rapid and significant pH falls because they most readily diffuse into the depths of plaque. In practical dietary terms it is sugars like sucrose, glucose and fructose which are most important in this regard. The acids involved can be identified, for example by gas liquid chromatography, in sugar-saliva mixtures, or after incubation of foodstuffs with saliva or plaque microorganisms and, with more difficulty, in dental plaque and carious enamel itself. There are many glycolytic bacteria in plaque and these include both homolactate fermenters and heterolactate fermenters. Lactate, acetate, propionate and other aliphatic acids are produced; but, of these, lactate is the most important both because it is produced in the largest quantities and because it is the strongest of these acids. It has been estimated (R.A.D. Williams, personal communication) that, if 50 per cent of bacteria in plaque are glycolytic, each milligram of plaque produces 102
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its own weight of lactic acid whilst growing to that weight on a carbohydrate substrate. A mouth may grow 10 mg of plaque per day but most of this acid is harmlessly diluted in saliva: it only requires a small percentage, however, if retained within the plaque, to produce a decalcifying pH. I have mentioned the importance of regional variation in plaque microflora. One such variation which has attracted attention is the presence of Veillonellae and the symbiotic relation between this species and several strains of streptococci. Veillonellae lack certain key enzymes of glycolysis and of the pentosephosphate pathway. They are, however, able to grow well in the presence of streptococci where they utilise the lactate produced by these organisms, generating propionic and acetic acids in the process. These latter acids are, fortunately, less strong than lactate, so that such mixed cultures result in less acid formation. Other acids are produced from protein catabolism by, for example, Bacteroides, but these make a minor contribution. Base is also produced, by decarboxylation of amino acids and hydrolysis of urea, so that alkaline conditions can exist in plaque and these circumstances favour its mineralisation to produce dental calculus. In general, however, nett acid production by plaque in stagnation areas utilising carbohydrate substrates is more usual.
The role of dietary carbohydrate: sucrose the ‘arch criminal’ The relative cariogenicity of different carbohydrates depends on frequency of intake, on their physical form - sticky, retentive substances such as toffee being worst - and on their chemical type. Complex carbohydrates such as starch are not digested to any significant degree in the mouth. Low-molecular-weight substances, particularly sugars, are more dangerous because they can more readily diffuse into the plaque and are more rapidly metabolised by the bacteria. Sucrose has been described as the ‘arch criminal’ of dental caries (Newbrun, 1967). It is much more cariogenic than glucose, for example, which diffuses just as readily into plaque and produces acid just as quickly. Sucrose is the most frequently consumed sugar in modern diets and some explanation of the mechanism by which it produces damage is now available. Cariogenic microorganisms synthesize extracellular polysaccharides faster from this disaccharide than from any other sugar; faster even than from equivalent mixtures of its constituents glucose and fructose. The energy liberated from rupture of the disaccharide bond is used, with the aid of bacterial glucosyl transferases, to synthesize complex polyglucans from the glucose. Fructose is synthesized to polyfructans of the levan type which are not so stable and may be converted to acid quite quickly. Plaque bacteria also make, and store, intracellular polysaccharides of the glycogen type from dietary sugars. Both intracellular and extracellular polysaccharides may be used as substrates for acid production in periods when n o food is being taken into the mouth. It is as important, therefore, to remove the bacteria as to restrict carbohydrate intake, and teeth might well be cleaned before meals with as much effect as after meals; indeed all our knowledge of the pathogenesis of caries points t o before-meal cleaning as the most rational oral hygiene approach to caries prevention. A number of studies have shown that the presence of sucrose in the diet favours the implantation of cariogenic streptococci into the mouths of rats, hamsters, monkey and man (eg, Huxley, 1974). 103
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Epidemiological evidence on the relation between diet and dental caries Several studies are frequently quoted under this heading for they have become classical pieces of evidence that diet has a profound influence on caries activity. In the 1930s the inhabitants of the isolated South Atlantic island of Tristan da Cunha lived on a diet of local vegetables, meat and fish and had excellent dental health. Increasing importation of manufactured foods in the intervening years led to increasing caries and finally, with the evacuation of the islanders to Britain, to marked caries incidence (Fisher, 1972). Caries incidence figures in children of several European countries during the second World War were significantly depressed in parallel with the reduced sugar consumption of that time. Once sweets were no longer rationed caries rapidly increased (Marthaler, 1967). Two longitudinal studies on institutionalised individuals have also become classics. The first of these is the Vipeholm study in which various groups of adults in a mental hospital were allowed access to table sugar and toffees in different amounts and at various frequencies. They had previously been shown, over a period of several years, t o have low caries on a nutritionally adequate diet low in carbohydrate. Caries increased significantly .when sucrose-containing foods were made available, particularly in those who consumed sucrose bet ween meals; sucrose confined to meal-times was far less dangerous. Furthermore, toffees which adhered t o the teeth and maintained high sucrose levels in saliva for prolonged periods were far more damaging than those which were rapidly 1954). cleared from the mouth (Gustaffson et d., The second is a study of 80 children raised at Hopewood House, New South Wales, Australia, on a vegetarian/dairy-product diet excluding refined carbohydrates. In spite of poor oral hygiene and low levels of fluoride in the water supply children in the 5-13 year age group had only about 10 per cent of the caries level of the general population. After leaving the home these same children rapidly developed caries, indicating that the caries protection was not a nutritional effect during tooth development (Harris, 1963). Individuals suffering from hereditary fructose intolerance provide another good example of the cariogenicity of sucrose and the relatively low cariogenicity of other carbohydrates. If children with this inborn error of metabolism are to survive they must avoid foods containing fructose and sucrose, though they can and do consume milk sugar (lactose) and starch. Such individuals have remarkably little - indeed often zero - caries (Linden & Nisell, 1964; Newbrun, 1967; Hess & Graf, 1975). A number of the above studies have recently been criticised by Jackson (1978); but, although he raises many valid qualifications, they do not detract from the overwheming weight of evidence that sugar causes caries. In addition to these observations on man there is a large literature o n the relative cariogenicity of different foodstuffs in animals, mostly rodents (see, for example Stephan, 1966; Bibby, 1975; Grenby, 1976). In general these confirm the importance of sucrose content, of physical texture and adhesiveness, and of the molecular weight of sugar polymers. It should be remembered that most fruits contain fermentable sugars and are therefore moderately cariogenic. This includes apples, which are ineffective in cleaning the teeth because they do 104
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not remove plaque (Marthaler, 1968: Longhurst & Berman, 1973); it is time this popular misconception was dispelled. This does not mean, however, that apple eating should be discouraged as apples are infinitely preferable snacks t o sucrosecontaining foods. Furthermore they promote salivary flow which must be beneficial. Nutritional factors of importance in resistance of the teeth to dental caries Systemic nutritional factors, as opposed t o local dietary Pactors which influence dental caries, operate at two levels; first, during the period of tooth formation, exerting their effects via the composition and structure of the teeth; secondly, throughout life by influencing the composition and flow of saliva. There is no doubt that the poor nutrition common in many of the world’s preindustrialised societies results in a relatively high prevalence of hypoplastic and hypomineralised defects in teeth (eg Infante & Gillespie, 1974; Enwonwu, 1978). For many years such teeth were thought t o be no more susceptible to caries than normal, or even to be caries resistant. It now appears that this was an erroneous impression, created by the low caries activity in these communities who did not eat cariogenic diets. Indeed recent work in Guatemala (Infante & Gillespie, 1977) shows that children with linear hypoplasia of anterior deciduous teeth had a significantly greater amount of caries in the apparently normal posterior dentition than did their peers who did not show hypoplastic defects. This suggests that the synergistic effect of undernutrition and infection, thought to be responsible for the enamel hypoplasia in the anterior teeth, predisposes clinically normal-looking posterior teeth to caries. Furthermore there are many reports of severely dysplastic teeth becoming seriously destroyed by caries (Sweeney, Saffir 8c de Leon, 1971), such misleading terms as ‘melanodontia’ (Mayer & Baume, 1966) or ‘odontoclasia’ (Jones, Larson & Prichard, 1930) having been applied t o this appearance in the past. The only nutritional factor of proven importance in influencing the canes resistance of teeth during their formation is fluoride. This acts partly by altering the shape of teeth, making them slightly smaller, with less plaque-retentive fissures and partly by making the hydroxy apatite crystals of enamel less soluble in organic acids by incorporation of F ions into the lattice (Levine, 1976; Murray, 1976). Other trace elements with a less marked effect are molybdenum and possibly also strontium, vanadium, lithium and boron (Navia, 1970; Curzon & Losee, 1977). Trace element effects apart, surprisingly little is known of what constitutes a ‘caries-resistant tooth’ (Ciba Symposium, 1965). It is probable that, in Western communities at least, intrinsic differences in susceptibility are swamped by the microbial/dietary/salivary interactions at the tooth surface. Finally, the nutritional quality of food must influence the function of salivary glands and thus the quality and flow rate of saliva (Dawes, 1970). Saliva is a highly important factor in the pathogenesis of caries and in oral defence mechanisms. Afiart from the diluting and washing effect saliva contains buffers; antibacterial factors like lysozyme and lactoperoxidase (Mandel, 1976); calcium, phosphorus, fluoride and other ions which inhibit tooth demineralisation; IgA 105
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which modifies bacterial colonisation of the tooth surface (Brandtzaeg, 1976); glycoproteins which contribute to pellicle and plaque formation (Bowen, 1976). Little is known, however, of how nutritional factors mediated via saliva influence caries activity. Relation between diet, nutrition and periodontal disease Because gingivitis and periodontitis represent an interaction between irritants derived from dental plaque and the host tissue response, nutritional effects on systemic health must be considered in conjunction with local dietary effects on plaque formation and bacterial metabolism. Severe protein-energy malnutrition and vitamin deficiencies certainly reduce the r’esistance of periodontal tissues to infection. Amongst the latter vitamin A, because of its importance to epithelial integrity, and vitamin C, because of its importance in collagen metabolism, are pahicularly important. It is not surprising, therefore, that conditions like acute necrotising ulcerative .gingivitis are more common in malnourished children of the low socio-economic groups in developing countries (eg, Enwonwu, 1978). Nonetheless, epidemiological surveys in many parts of the world have shown no significant correlation between nutritional status, as determined by biochemical tests, and the general level of periodontal disease (Russell, 1963); the relation between plaque volume and disease seems t o be dominant (Ramfjord, Kerr & Ash, 1966). Nevertheless, as Navia (1977) has argued, such studies have usually been made on advanced disease and nutritional effects on the all-important initial stages have been little studied. Furthermore the biochemical estimations of nutritional status are often single assessments made once disease is established and these tell us little of the situation during the initiation and progression of disease. Repair processes in periodontal tissues are bound to be influenced by nutrition, as is the host’s immune response to plaque antigens (see Susskind, 1977). The ecology of gingival plaque must be influenced partly by local dietary effects (Loesche, 1968) but until our knowledge of which organisms are important in the pathogenesis of periodontal disease improves, little can be concluded. Egelberg (1965) has shown that dogs on a hard diet containing large amounts of gristle have less plaque and less periodontal disease than those on softer diets of the same compositions but minced; it is doubtful if such large differences in texture apply to modern man. We have already seen that the occasional apple and carrot is ineffective in promoting an improvement in gingival health. The frequent intake of refined carbohydrate certainly promotes plaque formation in all the usual sites on the tooth surface, and thus promotes caries. Cariogenic diets are thus bound to promote periodontal disease also, but the association has not been closely investigated in man. The prevention of dental caries and periodontal disease From the above outline of the aetiology and pathogenesis of dental caries it is evident that attempts to break the complex sequence of events leading to disease can be directed at: 1. Dietary control (see below) 2. Plaque control : this includes a range of mechanical, chemical and immuno106
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logical methods for the removal of established plaque and the prevention of plaque growth. 3. Increasing the resistance of the tooth: this includes adequate nutrition during tooth formation, particularly the intake of optimum amounts of fluoride, the application of topical fluorides and remineralising solutions, and fissure sealants. Many of these methods will also help in the control of periodontal disease.
Theoretical approaches to the dietary control o f dental caries Space does not permit a detailed review of the literature concerned with dietary control of caries, though several aspects are covered in the subsequent papers. It is important t o ensure nutritional adequacy during growth and development of the teeth, and throughout life, so that salivary function and other body defences are maintained at optimal levels. Once the teeth have erupted we can attempt to break the chain of diet-related events leading to caries by: (1) Reducing the amount and frequency of intake of cariogenic carbohydrates; (2) modification of the form and texture of potentially cariogenic foods; (3) encouraging consumption of protective natural foods; (4) replacing sucrose in the diet with less cariogenic sweeteners; (5) adding cariesinhibitory substances to food. (1,2) : Controlling cariogenic foods. Measures here involve the restriction of sucrose to meal times, avoidance of adhesive fermentable carbohydrates, the limitation of between-meal snacks and the replacement of biscuits and the like with nuts, cheese, celery or apples. A valuable study of the effect on plaque pH of a range of British snack foods has recently been presented by Rugg-Gunn, Edgar & Jenkins (1978). (3): Protective natural foods. Animal experiments have shown that oat husks, wheat germ, raw molasses and chocolate contain protective factors. However, if man consumes these substances he does so in association with sucrose so that there is no beneficial effect. Dairy products, notably milk (McDougall, 1977) and cheese, are protective. This has considerable practical importance with respect t o meal patterns. For example if a cheese course is taken, in the French manner, before a sweet course, the pH fall in plaque as a result of the sweet is substantially reduced (Rugg-Gunn et at., 1975). Nuts o r a little cheese after a meal promote salivation which also reduces the pH drop (Geddes et al., 1977). (4): Sucrose substitutes. A substantial number of sucrose substitutes has been investigated and several have been commercially exploited (Newbrun, 19 73). These include cyclamates, saccharin, aspartame, sorbitol and xylitol. Most of these are inherently much sweeter than sucrose and can be used in small quantities. Nevertheless several are under suspicion as carcinogens, though in doses far in excess of those normally consumed by man. A further limitation is that most are vastly more expensive t o produce than sucrose. The agent attracting most current interest is xylitol, which has received extensive animal and human trials, particularly in Finland (Scheinin & Makinen, 1975; Makinen, 1978). 107
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(5): Food additives. Phosphate additives are thought to work on the principle of saturating plaque fluid with phosphate ions, inhibiting enamel demineralisation and favouring remineralisation by a mass action effect, and preventing depletion of plaque phosphate by the micro organisms during growth. Unfortunately the promise of animal experiments has not been borne out in man. Of the inorganic phosphates trimetaphosphate is apparently more effective than ortho-phosphate or pyro-phosphate (Harris, 1970a, b ) . Organic phosphates which have been studied include phytate, 0-glycerophosphate (Grenby & Bull, 1978) and calcium-sucrose-phosphate. The latter, under the trade name ‘Anticay’ has undergone extensive clinical trials in Australia but these are difficult to evaluate because some of the preparations also contained significant amounts of fluoride (Harris et aL, 1969). Finally fluoride may be delivered in foods, milk and table salt being the most commonly used vehicles. They are not as effective as water fluoridation but form a valuable alternative in communities resistant to the latter (see review by Murray, 1976). Bibliop a p hy More detailed coverage of many of the topics mentioned, together with fuller references, can be found in : Nizel, A.E. (1968) : The science of nutrition and its application in clinical dentistry. Philadelphia: Saunders. Caldwell, R.C. & Stallard, R.E. (1 977): A textbook of preventive dentistry. Philadelphia: Saunders. Jenkins, G.N. (1978): The physiology and biochemistry of the mouth, 4th edn. Oxford: Blackwell. Silverstone, L.M., Johnson, N.W., Hardie, J.M. & Williams, R.A.D. (1978): Dental caries: aetiology, pathology and prevention. London: MacMillan Press. Andlaw, RJ. (1977): Diet and dental caries - a review. J. Hum. Nutr. 31, 45-52. Levine, R.S. (1977): The aetiology of dental caries - an outline of current thought. Znt. Dent. J. 27, 341-348 Winter, G.B. (1976): Maternal nutritional requirements in relation to the subsequent development of teeth in children. J. Hum. Nutr. 31, 93-99
References Bibby, B.G. (1975): The cariogenicity of snack foods and confections. J. Am. Dent. Ass. 90, 121-132. Bowen, W.H. (1976): Nature of plaque. Oral Sci. Rev. 9, 3-21. Brandtzaeg, P. (1976): Synthesis and secretion of secretory immunoglobulins with special reference to dental caries. J. Dent. Res. 55, Special Issue C, 102-114. Ciba Foundation Symposium (1965): Caries resistant teeth. London: J. & A. Churchill. Cowley, G. & MacPhee, T. (1975): Essentials of periodontology and periodontics, 2nd edn. Oxford: Blackwell Scientific. Curzon, M.E.J. & Losee, F.L. (1977): Dental caries and trace element composition of whole human enamel. Eastern United States.J. A m . Dent. Ass. 94, 1146-1150. Dawes, C. (1970): Effects of diet on salivary secretion and composition. J. Dent. Res. 49, 1263-127 2. Egelberg, J. (1965): Local effects of diet on plaque formation and development of gingivitis in dogs. Odont. Revy 16, 31-60.
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Enwonwu, C. (1978): Interface of nutrition and dentistry in pre-industrialised tropical countries. Trop. Dent. J. 1, 19-44. Fisher, F.J. (1972): The pattern of dental caries in Trista da Cunha. DentalPractitioner 22, 267-270. Geddes, D.A.M., Edgar,W.M., Jenkins, G.N. & Rugg-Gunn, A.J. (1977): Apples, salted peanuts and plaque. Br. Dent. J. 142, 317-319 Gray, P.G., Todd, J.E., Slack, G.L. & Bulman, J.S. (1970): Adult dental health in England and Wales in 1968. London: Her Majesty’s Stationery Office. Grenby, T.H. (1976): Manufactured foods and dental decay. Nutr. Fd Sci. 45, 6-10. Grenby, T.H. & Bull, J.M. (1978): Dental caries in laboratory rats from breakfast cereals and its control by a calcium glycerophosphate additive. Archs Oral Biol. 23, 675-680. Gustafsson, B.E., Quesnel, C.E., Lanke, L.S., Lundqvist, C., Grahnen, H., Bonow, B.E. & Krasse, B. (1954): The Vipeholm dental caries study. The effect of different levels of carbohydrate intake on caries activity in 436 individuals observed for 5 years. Acta Odont. Scand. 11, 232-364. Harris, R. (1963): Biology of the children of HopewoodHouse, Bowral, Australia 4. Observations of dental caries experience extending over 5 years (1957-1961).J. Dent. Res. 42, 1387-1398 a r r i s , R., Schamschula, R.G., Beveridge, J. & Gregory, G. (1969): Calcium sucrose phosphate as a cariostatic agent in children aged 5-17 years: part IV. Aust. Dent. J. 42-49 Harris, R.S. (1970a):Fortification of foods and feed-products with anti-caries agents. J. Dent. Res. 49, 1340-44. Harris, R.S. (19706): Minerals: calcium and phosphates. I n Dietary chemicals us. dental caries, R.F. Gould (Ed). Amer. Chem. SOC:Advances in Science Series 94, 116-122 Hess, J. & Graf, H. (1975): Zahnplaque-pH bei Patienten mit hereditaren Fruktose-Intoleranz. Schweiz. Mschr. Zahnheilk. 85, 141-153. Huxley, H.G. (1974): The effect of dietary carbohydrate upon colonisation of plaque b y Streptococcus mutans in rats. Archs Oral Biol. 19, 941-946. [mfeld, Th., Hirsch, R.S. & Muhlemann, H.R. (1978): Telemetric recordings of interdental plaque pH during different meal patterns. Br. Dent. J. 144,40-45. [nfante, P.F., Gillespie, G.M. (1974): An epidemiological study of linear enamel hypoplasia of deciduous anterior teeth in Guatemalan children. Archs Oral BioL 19, 1055-1061. [nfante, P.F., Gillespie, R.M. (1977): Enamel hypoplasia in relation to caries in Guatemalan children. J. Dent. Res. 56, 493-498. Jackson, D. (1978): Sugar and dental caries: myth and fact. The Probe 19, 388-394. Jones, M.R., Larson, N.P. & Prichard, G.P. (1930): Dental disease in Hawaii - I: odontoclasia: a clinically unrecognised form of tooth decay in the pre-school child of Honolulu. Dent. Cosmos 72, 439-450. Keyes, P.H. (1960): The infectious and transmissable nature of experimental dental caries. Archs Oral Biol. 1, 304-326. Levine, R.S. (1976): The action of fluoride in caries prevention. A review of current concepts. Br. Dent. J. 140, 9-14. Linden, L. & Nisell, J. (1964): Hereditary intolerance to fructose. SvenskLakartidn. 61, 3185. Loesche, W.J. (1968): Importance of nutrition in gingival crevice microbial ecology. Periodontics 6, 245-249. Longhurst, P.L. & Berman, D.S. (1973): Apples and gingival health. Report of a feasibility study. Br. Dent. J. 134, 475-479. McDougall, W.A. (1977): Effect of milk on enamel demineralisation and remineralisation in vitro. Caries Res. 11, 166-172. Makinen, K.K. (1978): Biochemical principles of the use of xylitol in medicine and nutrition with special consideration of dental aspects. Experientia, Suppl. 30, in press. Mandel, I.D. (1976): Non-immunologic aspects of caries resistance. J. Dent. Res. 55, Special Issue C. 22-C31. Marthaler, T. (1967): Epidemiological and clinical dental findings in relation to intakes of carbohydrates. Caries Res. 1, 222-238. Marthaler, T. (1968): Apfel, Gesundheit und Kauorgan. Schweiz. Mschr Zahnhlk 78, 823-836. Mayer, J. & Baume, L.J. (1966): Pathologie de la melandontie infantile, de l’odontoclasie et de la carie circulaire. Rev. Suisse Odontol. 76, 48-92. 109
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Murray, J.J. (1976): Fluorides in caries prevention. In Dentalpractitioner handbook, No. 20. Bristol: Wright. Navia, J.M. (1970): Effects of minerals on dental caries. I n Dietary chemicals us dental caries. Am. Chem. SOC:Advances in Science Series No. 94. Navia, J.M. (1977): Nutrition and oral disease. In A textbook of preventive dentistry, ed Caldwell, R.C. & Stallard, R.E. Philadelphia: Saunders. Newbrun, E. (1967): Sucrose, the arch criminal of dental caries. Odont. Rev. 18, 373-386. Newbrun, E. (1973): Sugar, sugar substitutes and non-caloric sweetening agents. Int. Dent. J. 23, 328-345. Orland, F.J., Blayney, J.R., Harrison, R.W., Reyniers, J.A., Trexler, P.C., Ervin, R.F., Gordon, H.A. & Wagner, M. (1955): Experimental caries in germ-free rats inoculated with enterococci. J. A m . Dent. Ass. 50, 259-272. Pelton, W.J., Pennel, E. & Druzina, A. (1954): Tooth mortality experience of adults. J. A m . Dent. Ass. 49, 439. Ramfjord, S.P., Kerr, D.A. & Ash, M.M. (1966):.World workshop in periodontics.lJniv. of Michigan, Ann Arbor, Michigan. Rugg-Gunn, A.J., Edgar, W.M., Geddes, D.A.M. &Jenkins, G.N. (1975): The effect of different meal patterns upon plaque pH in human subjects. Br. Dent. J. 139, 351-356. Rugg-Gunn, A.J., Edgar, W.M. & Jenkins, G.N. (1978): The effect of eating some British snacks upon the pH of human dental plaque. Br. Dent. J. 145, 95-100. Russell, A.L. (1 963): International nutrition surveys: a summary of preliminary dental findings. J. Dent. Res. 42, 233-244. Scheinin, A. & Makinen, K.K. (1975): Turku sugar studies I-XXI. Final report on the effect of sucrose, fructose and xylitol diets on the caries incidence in man. Acta Odont. Scand. 33, Suppl. 70. Schluger, S., Yuodalis, R.A. & Page, R.C. (1977): Periodontal disease. Philadelphia: Lea & Febiger. Stallard, R.E. (1967): Current concepts of periodontal disease. J. Dent. Child. 34,204-210. Stephan, R.M. (1 944): Intraoral hydrogen ion concentrations associated with dental caries activity. J. Dent. Res. 23, 257-266. Stephan, R.M. (1966): Effect of different types of human foods on dental health in experimental animals. J. Dent. Res. 45, 1551-1561. Stratford, J.M. (1975): Gingivitis in school-age children: a review of the literature. J. Irish Dent. Ass, 21, 7-14. Susskind, R.M. Editor (1977): Malnutrition and the immune response. New York: Raven Press. Sweeney, E.A., Saffii, A.J. & de Leon, R. (1971): Linear hypoplasia of deciduous incisor teeth in malnourished children. A m . J. Clin. Nutr. 24, 29-31. Todd, J.E. (1975): Children’s dental health in England and Wales 1973. Office of Population. Censuses and Surveys. London: HMSO.
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