RECENT ADVANCES IN THE PREVENTION OF DENTAL CARIES

Postgraduate Lecture delivered at the Royal College of Surgeons of England on 29th April 1969 by

M. N. Naylor, R.D., B.Sc., Ph.D., B.D.S., F.D.S.

Reader in Preventive Dentistry, Guy's Hospital Dental School

Introduction RATIONAL PROCEDURES FOR the prevention of disease depend on an understanding of the aetiology and natural history of the disease; without such understanding preventive measures are empirical and without scientific basis. Whilst there are many aspects of the causation of dental caries which are not yet fully elucidated, it is not unreasonable to suggest that sufficient knowledge is now available to reduce considerably-if not prevent entirely-this widespread disease. In several respects, dental caries is an unusual disease; it has a predilection for Homo sapiens, though by dietary adjustments it can be induced in certain species of animal (Hartles and Lawton, 1957; Gustafson et al. 1955; Cohen and Bowen, 1966); it is a disease of so-called civilized man, and is virtually unknown in primitive communities; the disease has no reparative phase and once initiated the disease progresses until surgery, either by extraction of the tooth or excision of the diseased tissue, is carried out. The initiation of a caries lesion can be summarized by the chain reaction:
Mono- and disaccharides in the diet.

Uptake of these sugars by the dental plaque present in stagnation areas.

Degradation of sugars to form acid by plaque bacteria.
Acid accumulation causing fall in pH at plaqueenamel interface.
Acid dissolves enamel, thus initiation of the carious lesion.

Whilst this sequence represents a gross over-simplification, it can be readily appreciated that if the chain of events can be broken at one or more'points, then the caries process will be halted and lesions will not occur. The object of this paper is to assess the means of breaking the various links in this biological chain reaction. Dietary carbohydrates Since Miller's first report (1890), carbohydrates in the diet have been regarded as important aetiological considerations. However, only recently 305

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has it become accepted that short-chain carbohydrates, particularly the mono- and disaccharide hexoses alone have practical significance in caries initiation. It is certainly true that salivary bacteria under suitable laboratory conditions can degrade long-chain polysaccharides to produce acid, but it is highly unlikely that such a system is of any consequence under the conditions obtaining in vivo. Recent studies by Miihlemann and his colleagues (Graf and Muhlemann, 1966), using a telemetric technique to monitor pH on the tooth surface, have confirmed previous work of Stephan (1940) and Kleinberg (1961) demonstrating that sucrose and glucose either in solution or contained in sugary foods are degraded by bacteria to form acids in sufficient concentration to attack the surface of the enamel. These studies explain the findings of Gustafsson and his colleagues (1954), who carried out a two-year study of caries increments in subjects who were resident at the Vipeholm Psychiatric Hospital in Sweden. These subjects were divided into groups according to the nature of the calorific supplement to the basic diet. The data showed that those subjects who were given a daily supply of toffees which could be eaten at any time throughout the day had a far greater caries experience than those subjects who were on the control diet or diets involving sucrose supplements eaten at mealtimes only. Animal experiments reported by Konig et al. (1968) in which groups of rats were fed identical daily weights of high sucrosecontaining diets, but which were presented as 12, 18, 24 or 30 meals per day, showed that although the total amount of diet eaten per day was the same, the greater the frequency of mealtimes the greater was the amount of caries. Both of these studies indicate that, not only does the nature of the diet influence caries experience, but the pattern of eating is of importance too, and it is for this reason that it is sound clinical advice to confine consumption of fermentable sugar to mealtimes only. Many practitioners hold the view that bread is a cariogenic item of diet, white bread being more so than brown. No adequately controlled clinical study can be found to support this belief, and certainly the animal experiments carried out by Konig (1967) and Grenby (1967) showed that in rats all types of bread had low cariogenicity. Konig's work did show, however, that wholemeal whole corn bread induced more caries than wheat breads of 70 per cent and 82 per cent extraction. This was shown to be due to the increased vitamin B group content of the wholemeal bread, vitamins being of special importance for the efficient metabolic activity of the bacteria as well as the body as a whole. When sucrose was added to the breads the caries rate increased considerably. Bacterial plaque Bacterial plaque is a structure of slimy consistency which adheres tenaciously to the surface of a tooth. It can be removed by brushing or by means of scaling instruments, but it is unlikely to be washed off to 306

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any appreciable extent by jets of water or rough foods. As Bibby (1968) points out, the composition and nature of plaque varies considerably and it is quite unjustified to attribute to it uniformity of structure and function. It is justifiable to state, however, that plaque comprises a dense concentration of micro-organisms of many types, within a matrix containing extra-cellular polysaccharides, mostly of the dextran variety. The synthesis of these polysaccharides has been of considerable interest in recent years and evidence has been accumulating to show that they are synthesized by the bacteria of the plaque, mainly from sucrose in the diet (Carlsson and Egelberg, 1965). Gibbons and Baughart (1967) showed that cariogenic streptococci produced large amounts of dextran from sucrose. However, other hexoses appear able to be polymerized, at least by some plaque organisms (Naylor and Wilson, 1969). As was discussed previously, sucrose and other sugars are broken down to form acids capable of attacking enamel, but it was Miihlemann and his colleagues (Graf and Miihlemann, 1966) who showed that plaque is an essential requisite for this degradation to occur. It is therefore reasonable to suppose that any procedure which will either remove plaque or prevent it forming will be of practical value in the prevention of caries. Toothbrushing is a procedure long recommended by dental practitioners as a means of ensuring a healthy mouth. Whilst there is conclusive evidence that brushing is essential for the prevention, control, and indeed the treatment of periodontal disease, there is no satisfactorily controlled study reported in the literature which shows whether or not this procedure is of value in caries prevention. This is undoubtedly due to the extreme difficulty in designing and conducting a satisfactory study. On a priori grounds it can be argued that if all plaque is regularly removed from the pit and fissure regions, the approximal surfaces and cervical margins caries will not occur. However, few will dispute that this state is virtually impossible to attain, even by regularly applied oral hygiene methods. Fibrous foods of a detergent nature have long been advocated as a means of cleaning the mouth at the conclusion of a meal (Wallace, 1912). However, whilst these foods assist in the removal of food debris and sugar (Lundquist, 1952), they do not remove plaque. It is not surprising, therefore, that attempts have been made to find substances which will remove plaque or prevent plaque formation. Experiments have recently been reported on the use of dextranase, an enzyme produced by a culture filtrate of the fungi Penicilliumfuniculosum and lilacinium with dextrans as the filtrate. According to Guggenheim and Schroeder (1967) and Bowen (1968), inhibition of dextran synthesis by cariogenic streptococci growing in vitro on sucrose-containing media occurred in the presence of dextranase. In an animal study, Fitzgerald and his co-workers (1968) showed that both plaque deposits and caries 307

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were reduced when dextranase was included in the food and drinking water of rats. However, Konig and Guggenheim (1968) found that dextranase administered in the drinking water of rats in relative gnotobiosis caused no inhibition of plaque growth or caries, but when given in both food and water partial inhibition of fissure and smooth surface caries and plaque formation occurred. These findings are indeed interesting and of considerable importance but, before dextranase can be regarded as having a role in the prevention of caries, it is necessary to overcome the practical difficulties of including it in the diet-for example, like most enzymes it is heat labile-and it must be subjected to a properly conducted clinical study. At present, studies with monkeys are in progress in the Royal College of Surgeons' primate colony at Downe and the results of this work are awaited with considerable interest. Bacterial activity of the plaque Many attempts have been made to devise formulae to be used as toothpastes or mouthwashes which prevent decay by inhibition of bacterial fermentation of carbohydrates to organic acids capable of attacking enamel. Certainly many of these substances will inhibit oral bacterial activity in vitro, but, when subjected to full-scale controlled clinical trial, early promise has not been substantiated. In the past, suggestions have been made that caries might be controlled by means of a vaccine, but it is only recently that more precise identification of bacteria capable of initiating caries has made immunization a viable approach. Animal experiments by Bowen (1969) have shown that, in monkeys, administration of vaccine of whole live dextran-producing cariogenic streptococci caused substantially fewer carious lesions than in the control unvaccinated animals. The cariogenic organism, however, remained present in the mouth throughout the experiment, suggesting that any antibodies induced were not antibacterial. Antibiotics have been suggested as capable of reducing the activity of cariogenic organisms, but unless such a drug evolves which is devoid of unwanted side-effects, i.e. organisms do not become resistant and the subject does not become sensitized, then this group of drugs is unlikely to have any practical value. Acid production Clearly if some method could be devised to neutralize the acids produced in the plaque by microbiological fermentation of carbohydrates, acid attack of the enamel surface would not occur. No doubt this argument has formed the basis upon which a number of commercially prepared alkaline toothpastes and mouthwashes have been formulated. Whilst there is no report in the literature of such products being subjected to clinical trial, it seems unlikely that they could exert any practical 308

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beneficial effect, largely on account of the fact that the antacid agent must pass through the thickness of the plaque to reach the plaque-enamel interface. The evidence indicates that plaque is a structure of low diffusivity (Critchley et al. 1967) and therefore it seems unreasonable to speculate that neutralizing agents of any kind, including saliva, can diffuse through the plaque in sufficient concentration to influence materially the hydrogen in concentration at the plaque/enamel interface.

Protection of the enamel against acid attack Much has been written in the past about ways in which enamel formation, and its subsequent resistance to acid attack, can be influenced by dietary factors. However, apart from fluorides there is no unequivocal evidence that different dietary regimes can exert a systemic influence on the susceptibility or resistance of a tooth to caries.
Fluoridation

The effectiveness of a fluoride concentration of 1 p.p.m. naturally present in the drinking water in ensuring a reduced caries experience in children is well documented (Trendley Dean et al. 1942). Although some studies have suggested that fluorides present in the water at this optimum concentration merely effect a postponement of the onset of caries (Weaver, 1944), a detailed study by Russell and Elvove (1951) showed that the phenomenon of caries inhibition continued through to at least the fifth decade of life. Fluoridation of the public water supplies, i.e. adjustment of the fluoride ion concentration to 1 p.p.m. by the addition of fluoride compounds, was introduced in the U.S.A. soon after the end of World War IL, but since then many fluoridation schemes have been established in different parts of the world. In 1945 the community drinking water of Grand Rapids in the State of Michigan, U.S.A., was adjusted to 1 p.p.m. F and after 11 years (Arnold, 1957) it was shown that children 4-15 years old who were permanently resident in the area experienced a reduction in caries of the order of 60 per cent. The caries experience was similar to that produced by water with fluoride naturally present at a comparable level. The Evanston, Illinois, study (Blayney and Hill, 1967) showed similar reductions in children drinking artificially fluoridated water for 14 years. In Britain the results of the Anglesey, Kilmarnock and Watford studies were reported in 1962 (Ministry of Health) and it was shown that five years' fluoridation of drinking water caused a 50 per cent reduction in caries of deciduous teeth of five-year-old children and a considerable increase in caries-free mouths. The second report giving the findings after 11 years, published by the Department of Health in 1969, confirms the findings of previous reports from Britain, U.S.A. and elsewhere, and in addition shows that discontinuation of fluoridation in Kilmarnock in 309

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1961 has resulted in an increase in caries experience now approaching the pre-fluoridation level. The mechanisms by which fluorides prevent decay are not fully elucidated, but the various theories put forward have been critically evaluated by Jenkins (1966, 1967). Apart from fluoridation of the public water supplies, fluorides may be administered in other ways. Tablets, each containing 2.21 mg. of sodium fluoride in a soluble base, are available for home fluoridation. When dissolved in 1 litre of low fluoride-containing tap water a concentration of approximately 1 p.p.m. F ion is obtained, and it seems reasonable to suppose the effect of regular consumption of such water by children throughout life would be similar to fluoridation of public water supplies. Marthaler (1967) reported a study in which children aged 6-7 years were given a fluoride tablet daily and the caries experience of the upper and lower right first molars recorded. Although the crowns of these teeth were completely mineralized at the start of the study, by the age of 14-15 years these children had a reduced caries experience when compared with the control children who did not have the tablets. Smooth enamel surfaces showed a reduction of the order of 50 per cent, but when the pits and fissures were considered the reduction was much less spectacular. This finding that smooth surface caries is prevented to a greater extent than that of pits and fissures is in accordance with observations of Backer Dirks (1967), in respect of fluoridated public water supplies. Studies have been reported in which fluorides were incorporated into domestic salt (Marthaler, 1961) and into milk (Rusoff et al. 1962; Wirz, 1964). Cariostatic effects occurred with both methods, but the reductions were consistently less impressive than those obtained with public water fluoridation. Clearly the administration of fluorides in the home either with tablets, milk or salt places added burdens on the parents, and it is not unreasonable to suppose that many abandon the procedure simply on the grounds of its tedious nature. Topical application of fluorides painted on the teeth by the dental surgeon has long been advocated and according to Torell and Ericsson (1967) their value has been amply confirmed. A variety of solutions of various strengths have been advocated, amongst which are 2 per cent sodium fluoride (Knutson et al. 1947), 8 per cent stannous fluoride (Muhler, 1958) and 1.23 per cent acidulated fluoride-phosphate solution (Wellock and Brudevold, 1963). Such topical procedures are timeconsuming, but there is good evidence that they effectively reduce caries experience, especially in children with high caries activity (Torell and Ericsson, 1967). Mouth rinsing with fluoride solutions has been shown to be both effective and feasible as a group-conducted procedure. Solutions used 310

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include 10 ml. of 0.05 per cent solution of sodium fluoride used daily, or 10 ml. of 0.2 per cent solution of sodium fluoride used weekly. The solution is bubbled round the mouth and then spat out, but if inadvertently swallowed the solution is quite harmless. The value of this procedure is shown by the findings of a study reported by Torell and Siberg (1962) and Ollinen (1966), who reported a redu_tion of approximately 50 per cent of fillings required in Gothenburg schoolchildren after 5j years of fortnightly rinsing with a 0.2 per cent solution of sodium fluoride. Fluoride-containing dentifrices have commanded considerable attention during the last few years since Crest, a stannous fluoride formulation, made its appearance, first in 1955 on the U.S.A. market and later on the British. Reductions in caries experience of the order of 50 per cent have been claimed for this paste (for brief review of these U.S.A studies see Jackson et al. 1967). In order to test the value of fluoride-containing pastes under conditions obtaining in Britain, a series of clinical trials was set up in this country. In all, five studies were begun in 1961; all were conducted independently, but there was considerable discussion between the various examiners on such matters as experimental design, diagnostic and radiographic criteria, and management and presentation of data. The various formulae tested were a stannous fluoride and dicalcium pyrophosphate preparation (Slack et al. 1967a; James and Anderson, 1967; Jackson and Sutcliffe, 1967), stannous fluoride and insoluble sodium metaphosphate preparation (Slack et al. 1967b), stannous fluoride and insoluble metaphosphate, and sodium monofluorophosphate and dicalcium phosphate preparations (Naylor and Emslie, 1967). These studies which continued over a three-year period and were carried out using the doubleblind controlled technique on children aged 11-12 years at the beginning of the study who were not supervised in the use of the toothpastes. All studies save one (Jackson and Sutcliffe, 1967) included an annual 'bitewing' radiographic examination of the posterior teeth. In all studies a significant reduction in caries experience, as compared with the controls, was demonstrated. In one of the studies (Naylor and Emslie, 1967) it was shown that teeth which erupted during the course of the trial benefited to a greater extent than teeth which had erupted earlier. Although the reduction in caries experience associated with the use of fluoride-containing toothpastes did not anything like match the reduction caused by fluoridation of water supplies, when used regularly and conscientiously, they can play an important part in the control and prevention of caries, especially in children when teeth are erupting. Summary and Conclusions In this review the various established methods of controlling and preventing dental caries have been evaluated and an attempt made to assess their merits as a practical dental health measure. Dental caries experience can be reduced considerably by controlling the intake of fermentable carbohydrates, confining their consumption to 311

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mealtimes only. Evidence is offered suggesting that sucrose is particularly likely to cause caries because not only can it be fermented to form acids, but it can also be synthesized to form extra-cellular polysaccharides of the dextran type. Consideration is given to the various ways of employing fluorides and the conclusion reached that, whilst other procedures may be helpful, adjustment in the fluoride ion content of the public water supplies to 1 p.p.m. is by far the most efficient method of reducing decay.
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ARNOLD, F. A. (1957) Amer. J. publ. Hlth. 47, 539. BACKER DIRKS, 0. (1967) Int. dent. J. 17, 582. BIBBY, B. G. (1968) Caries Reg. 2, 97. BLAYNEY, J. R., and HILL, I. N. (1967) J. Amer. dent. Ass. 74, 246. BOWEN, W. H. (1968) Brit. dent. J. 124, 347. (1969) Brit. dent. J. 126, 159. CARLSSON, J., and EGELBERG, J. (1965) Odont. Rev. 16, 112. COHEN, B., and BOWEN, W. H. (1966) Brit. dent. J. 121,269. CRITCHLEY, P., WOOD, J. M., SAXTON, C. A., and LEACH, S. A. (1967) Caries Res. 1, 112. DEAN, H. TRENDLEY, ARNOLD, F. A., and ELVOVE, E. (1942) U.S. pub!. Hith. Rep. 57, 1155. DEPARTMENT OF HEALTH AND SOCIAL SECURITY, SCOTrISH OFFICE, MINISTRY OF HOUSING AND LOCAL GOVERNMENT (1969) The Fluoridation studies in the U.K. and the results achieved after 11 years. Rep. publ. Hith. med. Subj. 122. London, H.M.S.O. FITZGERALD, R. J., KEYES, P. H., STOUDT, TH. H., and SPINELL, D. M. (1968) J. Amer. dent. Ass. 76, 301. GIBBONS, R. J., and BAUGHART, S. B. (1967) Arch. oral Biol. 12, 11. GRAF, H., and MUHLEMANN, H. R. (1966) Helv. odont. Acta. 10, 94. GRENBY, T. H. (1967) Carieg Res. 1, 208. GUGGENHEIM, B., and SCHROEDER, H. (1967) Helv. odont. Acta, 11, 131. GUSTAFSON, G., STELLING, E., ABRAMSON, E., and BRUNIUS, E. (1955) Odontol. Tidskr. 63, 506. GUSTAFSSIN, B. E., QUENSEL, C. E., SWENLANDER, L. L., LUNDQUIST, C., GRAHNEN, H., BoNow, B. E., and KRASSE, B. (1954) Acta odont. scand. 11, 232. HARTLES, R. L., and LAWTON, F. E. (1957) Brit. J. Nutr. 11, 13. JACKSON, D., JAMES, P. M. C., and SLACK, G. L. (1967) Brit. dent. J. 123, 16. and SUTCLIFFE, P. (1967) Brit. dent. J. 123, 32. JAMES, P. M. C., and ANDERSON, R. J. (1967) Brit. dent. J. 123,25. JENKINS, G. N. (1966) Physiology of the Mouth, 3rd edit. Oxford, Blackwell. (1967) Int. dent. J. 17, 552. KLEINBERG, I. (1961) J. dent. Res. 40, 1087. KNUTSON, J. W., ARMSTRONG, W. D., and FELDMAN, F. M. (1947) U.S. publ. Hlth. Rep. 62,425. KONIG, K. G. (1967) Brit. dent. J. 123, 585. and GUGGENHEIM, B. (1968) Helv. odont. acta, 12, 48. SCHMID, P., and SCHMID, R. (1968) Arch. oral Biol. 13, 13. LUNDQUIST, C. (1952) Ondont. Rev. 3, Suppl. 1, 5. MARTHALER, T. M. (1961) Schweiz. Mschr. Zahnheilk. 72, 754. (1967) Int. dent. J. 17, 606. MILLER, W. D. (1890) Microorganisms,ofthe Human Mouth, Philadelphia, Pennsylvania: S. S. White Pub]. Co. MINISTRY OF HEALTH, SCOlTISH OFFICE, MINISTRY OF HOUSING AND LOCAL GOVERNMENT (1962) The Conduct of Fluoridation Studies in the U.K. and the results achieved after 5 years. Rep. publ. Hlth. med. Subj. 105. London, H.M.S.O. MUHLER, J. C. (1958) J. dent. Child. 25, 306. NAYLOR, M. N., and EMSLIE, R. D. (1967) Brit. dent. J. 123,9. and WILSON, R. F. (1969) Unpublished data. OLLINEN, P. (1966) Sver. Tandlak-Forb. Tond. 58, 913.

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RECENT ADVANCES IN TH1E PREVENTION OF DENTAL CARIES RuSoFF, L. L., KONIKOFF, B. S., FRYE, J. B., JOHNSTONE, J. E., and FRYE, W. W. (1962) Amer. J. clin. Nutr. 11, 94. RUSSELL, A. L., and ELVOVE, E. (1951) U.S. publ. Hith. Rep. 66,1389. SLACK, G. L., BERMAN, D. S., MARTnN, W. J., and YOUNG, J. (1967a) Brit. dent. J. 123, 1. and HARDIE, J. M. (1967b) Brit. dent. J. 123, 18. STEPHAN, R. M. (1940) J. Amer. dent. Ass. 27, 718. TORELL, P., and ERICSSON, Y. (1967) Int. dent. J. 17, 564. and SIBERG, A. (1962) Odont. Rev. 13, 62. WALLACE, J. SIM. (1912) Prevention of Common Diseases of Childhood. London, Bailli6re. WEAVER, R. (1944) Brit. dent. J. 76, 149. WELLOCK, W. D., and BRUDEVOLD, F. (1963) Arch. oral Biol. 8, 179. WIRz, R. (1964) Schweiz. Mschr. Zahnheilk. 74, 658.

PROCEEDINGS OF THE COUNCIL IN OCTOBER AT A MEETING of the Council on 9th October 1969, with Sir Thomas Holmes Sellors, President, in the Chair, Mr. S. H. Harrison, F.R.C.S.Ed., of Windsor, was elected to the Fellowship ad eundem. Group-Captain J. N. C. Cooke, O.B.E., M.R.C.S., F.R.C.P., of Princess Alexandra's Royal Air Force Hospital, Wroughton, was awarded the Lady Cade Medal for 1968. Colonel M. M. Lewis, M.D., M.Sc., D.P.H., D.T.M. & H., D.I.H., Director of Army Health with the Australian Military Forces, was awarded the Mitchiner Medal for 1970. The appointment of Professor G. S. Brindley, F.R.S., M.R.C.S., of the Institute of Psychiatry, as the Edridge-Green Lecturer for 1969 was reported. Mr. Norman Capener, C.B.E., F.R.C.S., was appointed the Honorary Curator of Portraits and Paintings. Diplomas of Fellowship in the Faculty of Anaesthetists were granted to the candidates named on page 315. Diplomas of Fellowship were granted to C. G. C. Gaches and R. M. P. Reynolds. A Diploma of Fellowship in Dental Surgery was granted to Y. A. Liok. Ten Diplomas of Membership were granted. One Licence in Dental Surgery was granted. Diplomas in Dental Public Health were granted to 26 candidates. The following Diplomas were granted, jointly with the Royal College of Physicians: Industrial Health (6), Ophthalmology (45), Tropical Medicine and Hygiene (44), Anaesthetics (3), Psychological Medicine (1), Medical Radiotherapy (1). 313