Fluoride in Dental Plaque and its Effects A. TATEVOSSIAN 18 Thornhill Road, Cardiff CF4 6PF, Wales, United Kingdom Total plaque fluoride is in the range 5-10 mgfkg (ppm) on a wetweight basis. The variability of literature data on plaque fluoride is partly ascribed to analytical problems, many assays being close to or below the concentration detection limit of the fluoride electrode. A change in classification ofplaque fluoride compartments is necessary, since recent work indicates that there are two pools ofplaque F: 95% extractable by cold 0.5 molll: perchloric acid. Sources of plaque fluoride include the diet, saliva, and crevicular fluid; enamel is unlikely to be a regular source for plaque F unless it is either coated daily with labile fluoride compounds, such as calcium fluoride, or released by demineralization. The location and nature ofplaque bound F are not established, but the present evidence is consistent with an intracellular location. Bound F may be released by acids produced in plaque during sugar fermentation, but it is unlikely to reach ion concentrations high enough for sufficient time periods to exert significant inhibition of plaque acidogenesis. Epidemiological evidence showing correlations between pooled plaque F concentrations and caries prevalence in the plaque donors does not exclude the possibility ofcoincidental effects of water F on both caries and plaque F concentrations. The action of F in reducing caries has been considered to depend on a multiplicity ofeffects on enamel and dental plaque, but the range of F concentrations used for such effects in dental plaque spans five orders of magnitude. Of these, only F effects in enhancing enamel remineralization and reducing the solubility rate for enamel mineral appear likely to be of practical importance. Cationic fluoride preparations containing metal ions can reduce plaque formation in the short term, but the effect is manifested mainly by the cation rather than by the F. However, progress has been made in formulation of rinse solutions which can raise plaque fluoride levels (as well as calcium and phosphate) long enough to reduce plaque acidogenicity and its potential to demineralize enamel during fermentation.
J Dent Res 69(Spec Iss):645-652, February, 1990
Introduction. Research has continued to seek answers to some of the questions raised in the previous Workshop on Cariostatic Mechanisms of Fluorides (Jenkins and Edgar, 1977). Reviews have appraised some of these questions (Tatevossian, 1980; Edgar, 1981; Geddes and Rolla, 1988), and some of the material therein is included in this presentation where appropriate.
in F concentration. Theoretically, the detection limit is determined by the solubility of the europium-doped lanthanum fluoride crystal, but estimates of the solubility product have ranged from 3.3 X 10- 25 to 7 X 10- 17 (Moody and Thomas, 1971). In practice, the detection limit for F is close to 1 umol/L (0.019 ppm F), and most commercial electrodes show both a nonlinearity in Nernstian response in the range below 5 urnol/L (0.095 ppm F) as well as considerable slowing in electrode 99% response time in this range. Birkeland and Speirs (1977) pointed out that despite the improved method of measuring fluoride ion, analyses of dental plaque have often been carried out at the limit of sensitivity of the electrode and without giving calibration data at this analytically marginal level. This still seems to be the case when average F concentrations of reaction mixtures measured with the electrode are calculated from the literature (Table 2). The data in Table 1 should be evaluated by reference to Table 2 where possible. Some of the data (Table 1) are based on analyses close to or below the detection limit of the electrode (Table 2) and should be considered approximate rather than absolute. It is thus not prudent to give a definitive value for plaque F, although most estimates of plaque total F are in the range 5-10 mg F/kg wet weight (or ppm F). Comparatively higher values are found in plaque from subjects receiving fluoridated water (Table 1), including the few reports on plaque fluid F. Isotachophoresis and ion chromatography are at about the same level of sensitivity as the F electrode and to date have not been exploited to any significant extent (Geddes and Rolla, 1988). Analytical problems have also beset the reliable description of the compartments of F in plaque. Until recently, most workers believed that total plaque F could only be obtained after digestion in hot acid (Jenkins and Edgar, 1977; Edgar, 1981; Geddes and Rolla, 1988). Ophaug et at. (1987) confirmed an earlier report by Gaugler and Bruton (1982) that cold perchloric acid removed >95% of plaque total F (Table 1), and it may now be unsound to distinguish between plaque F compartments on the basis of their extraction by different reagents and conditions. The implications of this finding are discussed in more detail below.
Sources of plaque fluoride. Analytical considerations. The use of the fluoride electrode in the late 1960's heralded a significant advance over earlier colorimetric methods for fluoride analysis in dental plaque (Singer and Armstrong, 1965; Gren et al., 1969). Most F-electrode estimates of the total fluoride concentration in plaque tend to be 2-5 times lower than those from colorimetric assays (Table 1). The potentiometric F analysis implies an order of magnitude increase in sensitivity with each order of magnitude decrease Presented at a Joint IADR/ORCA International Symposium on Fluorides: Mechanisms of Action and Recommendations for Use, held March 21-24, 1989, Callaway Gardens Conference Center, Pine Mountain, Georgia
Jenkins and Edgar (1977) reviewed this topic and concluded that the diet and saliva, but not enamel, are sources of plaque fluoride. Usually, enamel is unlikely to be a source for plaque F, and the reverse has been proposed (Charlton et al., 1974), especially on cervical enamel surfaces habitually covered by plaque (and possibly demineralized by plaque) where F is higher (Weatherell et al., 1972, 1977). Were enamel F the usual source for plaque F, regular toothbrushing with F-free toothpaste, as in the data of Weatherell et al., would have depleted F in cervical enamel. The reverse was found to be the case. However, under demineralizing conditions, it is possible to demonstrate an in vitro uptake of fluoride from enamel by thick films of Streptococcus mutans FA1 (Klimek et al., 1983). However, this could not occur repeatedly without depleting enamel fluoride, which has not been found to be the case on 645
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TABLE 1 SOME ESTIMATES OF FLUORIDE IN DENTALPLAQUE(Mean ± SD)
Wet (W) or dry (D) weight basis
Low
Pre-electrode (mglkg) Hardwick & Leach (1962) D W Dawes et al. (1965) Post-electrode Plaque fluid F (}JJ1lol/L) Edgar & Tatevossian (1971) Hassell et aI. (1971) Shields & Muhlemann (1975) Tatevossian & Gould (1976) Tatevossian (1978) Carey et aI. (1986) Bound F (mgfkg wet [Wi or dry [D] weight) from cold acid extracts Gren et al. (1969) W D Brown et al. (1981) W W Gaugler & Bruton (1982) Geddes & McNee (1982) W W Grobler et aI. (1982) W Brown et aI. (1983) D Pearce (1984) Duckworth et aI. (1987) W W Ophaug et al. (1987) D Nobre dos Santos & Cury (1988) Total F (mg/kg wet [Wi or dry [D] weight) from hot acid digests Singer et al. (1970) W D Birkeland et al. (1971) D Agus et al. (1976) Schamschula et aI. (1977) D W Turtola (1977) D Tatevossian (1978) W Agus et aI. (1980) Rugg-Gunn et aI. (1981) W W Geddes & McNee (1982) W Gaugler & Bruton (1982) W Ophaug et al. (1987) D Wilson & Ashley (1988) D
-100 umol/L (-2 ppm) 235 47 :!: 22
125 25 ± 17 -29 12 (wet) 3.3 (dry)
Pearce (1984) Duckworth et al. (1987) Ophaug et al, (1987) Nobre dos Santos & Cury (1988)
in in in in in in in in
Average F Concentration (urnol/L) in Analyzates
1.5 mL 1.2 mL 0.4 mL 0.1 mL 1 mL 0.2 mL 1 mL 1 mL
in 1 mL in 1 mL in 1 mL in 1.3 mL in 0.2 mL in 1 mL in 1 mL
2.9 0.7 (low F) 1.4 (high F) 1.3 3.3 38.6 12.7 1.5 5.1
2.5 0.6 (low F) 1.6 (high F) 0.7 1.0 '70.1 0.3 52.6 > 1.1 3.8
'Mineralized plaque.
(> 95%) by cold 0.5 mol/L perchloric acid, and since the ionized F in plaque fluid constitutes 10 times the concentrations reported in plaque fluid (Table 1). There is a lack of data on the F concentrations in plaque fluid during sugar fermentation. Turtola (1977) calculated from plaque extracts that ionized F may rise to - 50 umol/L in plaque during daily ingestion of 10 x 2 g tablets of sucrose. If the entire plaque F (- 5 mglkg wet weight; Table 1) were released during fermentation, the F concentration in plaque fluid is unlikely to exceed 1 mmol/L, and the rapid decline of soluble F in plaque (see below) implies that bacterial inhibition would be too short-lived even in these circumstances.
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Can plaque F concentrations approach those for currently proposed mechanisms of action of plaque F? Although the therapeutic action of fluoride in reducing the incidence of dental caries has been considered to depend on a multiplicity of effects on the enamel and dental plaque, demonstrations of some of these effects have spanned several orders of magnitude in fluoride concentration (Table 4, based on Tatevossian, 1980). Plaque appears not to reduceenamel uptakeof F from rinses (review by Ripa, 1984), although MFP uptake is enhanced, presumably by enzymatic hydrolysis in dentalplaque(Jackson, 1982; Ogaard et al., 1985; Hellwig et al., 1987; Briiun et al., 1987). The reduction in plaque deposits by stannous or aminefluoride either in rinses or toothpaste is a clinically significant effect at - 5 mmol/L (Table 4), albeit being based on the cation rather than on the Fanion (Tinanoff and Weeks, 1979; Shern et al., 1970). Surprisingly, stannous fluoride has no demonstrable anti-plaque effect after 16 months' continuous use as a mouthrinse (Leverett et al., 1984) and may cause a rise in salivarylactobacillus counts(Svanberg and Westergren, 1983). Whether bound F inhibits plaque metabolism remains questionable, as does the possibility that such effects are exhibited by F released during fermentation. In plaque not containing native or introduced mineral, such release appears unlikely to achieve concentrations of F in plaque fluid for periods of time sufficient to inhibit bacterial metabolism, or indeed to achieve most of the effects proposed for plaque F (Table 4), exceptfor enamel remineralization and a reduced solubility rate for enamel hydroxyapatite.
Can bound F be increased in dental plaque by topical means in order to reach therapeutically significant levels? The kinetics of soluble inorganic F in dental plaque is too rapid to allow a significant build-up of F using conventional rinses(Table 5). In the studyby Birkeland et al. (1971),plaque F was abovebaselinevalues 24 h after a rinsewith NaF (Table 5), which is contraryto the general trend of other studies (Table 5). However, the plaqueweightsfor four-hour and 24-hour samples were lower than those of the 2-4-day samples (thus tending to give higher F values), while the five-day samples, which were as low in average weight as the 24-hour samples, also demonstrated high F values. Even though these were not statistically above the baseline values, they were in the same range as the 24-hour data (which were statistically above baseline values). These authors noted that, with increasing weight of deposits, the F concentrations decreased. Moreover, the
average dry weights of all their samples (see Table 2) were low, in the range 1.12 mg (four-hour samples) to 1.67 mg (three-day sample). Hassell et al. (1971) ascribed the rapid kinetics of free F in plaque (Table 5) to bindingwithinplaque but gave no evidence to substantiate this conclusion. In four- or five-day control plaque, F activity was as high as 100 urnol/L or greater (Shields and Miihlemann, 1975). These data suggest the need for caution in the interpretation of telemetric data. Single daily mouthrinses over a period of four weeks were reported to cause small increases of bound F in plaque collected > 18 h after the last application (Duckworth et al., 1987; Table 5). The range of plaque bound F was low, however 1.2 ppm in controls, and 3.3 ppm four weeks after use of 0.053 mol/L F (Table 1) - and their analyzate concentrations were on average below the detection limit for the F electrode (Table 2). A marked fall in plaque boundF following cessation of fluoridation was reported in Brazilby Nobredos Santosand Cury (1988). However, their post-fluoridation values (Table 1) are the lowestyet reported in dental plaque (1.7 :+: 0.6 SD mg/kg dry weight). In contrast to the modest and short-lived effects of soluble fluoride (Table 5), therapeutically significant levelsof fluoride as well as calcium and phosphate were shown to be retained > 16 h in dental plaque following rinses (four times daily) with a mouthrinsecontaining urea, calcium,phosphate, and fluoride (Pearce, 1984; Table 5). Pearce et al. (1984) showed that loading plaquewith mineral could lower its acidogenicity (Table 3) and reduceits softening effecton bovine enamel in vitro. Clinical trials are needed to evaluate the caries-preventive efficacy of this formulation. We have much yet to learn about the dynamics of fluoride in dental plaque at different sites in the mouth under fluctuating intra-oral conditions.
Implications for the rational use of fluorides. Cationic fluoride preparations containing metal ions are effective in the short term in reducing plaque formation (Table 4). The presence of plaque during topical treatments may be advantageous and is not detrimental to the efficacy of fluoride uptake by enamel or F effects on mineral turnover. Fluoridationof the waterseems to be a mechanism for increasing plaque F. The evidence for the effect of fluoride, as distinct from metal ions, in inhibiting plaque metabolism is far from being conclusive and, at most, suggests that a smalleffect is possible for short periods after pulsing plaque with high F concentrations. There are prospects for developing fluoride preparations which can be retained in dental plaque at therapeutic concentrations for sufficiently long to be beneficial. REFERENCES AGUS, H.M.; UN, P.S.H.; COOPER, M.H.; and SCHAMSCHULA, R.G. (1980): Ionized and Bound Fluoride in Resting and Fermenting Dental
TABLE 4 FLUORIDEEFFECfS DEMONSTRATED AT DIFFERENT CONCENTRATIONS Concentration (mol/L) 0.5
5 X 10- 3 1 X 10- 3 5 X 10-' 5 X 10-s 5 X 10- 6
Effect Desorptionof bacteria from apatite Reduction in plaque formation Desorption of albumin from apatite Inhibition of bacterial metabolism Fluoridation reduces dental caries and may affect fissure morphology Reduces solubility rate of apatite Enhances remineralization of apatite
Reference Rolla & Melsen, 1975 Tinanoff and Weeks, 1979 Rolla & Melsen, 1975 Hamilton, 1977 Johansen et al., 1979 Thiradilok & Feagin, 1978
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PLAQUE FLUORIDE
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TABLE 5 KINETICS OF FLUORIDE IN DENTAL PLAQUE Concentration
Duration of Elevated Plaque F
(rnol/L) 0.05 NaF 0.05 NaF 0.05 NaF weekly 0.05 NaF 0.05 NaF Not Known
0.02 NaF 5-26 X 10- 5 NaF in milk 0.048 NaF 0.005,0.013 or 0.053 NaF daily for 4 weeks 0.005 MFP + NaF 4 x daily rinse with mineralizing solution
Reference
60% above baseline 24 h later mostly eliminated within 1 h 2 x above baseline after 1 day 1 h (4- or 7-day plaque) No elevation during eating 2 g sucrose + 50 or 20 ug F as NaF 16 h
Pearce, 1984
Plaque and Individual Human Caries Experience, Arch Oral Bioi 25:517522. AGUS, H.M.; SCHAMSCHULA, R.G.; BARMES, D.E.; and BUNZEL, M. (1976): Associations Between the Total Fluoride Content of Dental Plaque and Individual Caries Experience in Australian Children, Community Dent Oral Epidemiol 4:210-214. BIRKELAND, J.A. (1970): Direct Potentiometric Determination of Fluoride in Soft Tooth Deposits, Caries Res 4:243-255. BIRKELAND, J.M. and CHARLTON, G. (1976): Effect of pH on the Fluoride Ion Activity of Plaque, Caries Res 10:72-80. BIRKELAND, J.M.; JORKJEND, L.; and VON DER FEHR, F.R. (1971): The Influence of Fluoride Rinses on the Fluoride Content of Dental Plaque in Children, Caries Res 5:169-179. BIRKELAND, J.M. and ROLLA, G. (1972): In vitro Affinity of Fluoride to Proteins, Dextrans, Bacteria and Salivary Components, Arch Oral Bioi 17:455-463. BIRKELAND, J.M. and SPEIRS, R.L. (1977): Discussion, Caries Res 11 (Suppl. 1):237-242. BROWN, L.R.; WHITE, 1.0.; HORTON, I.M.; DREIZEN, S.; and STRECKFUSS, J.L. (1983): Effect of Continuous Fluoride Gel Use on Plaque Fluoride Retention and Microbial Activity,J Dent Res 62:746-751. BROWN, L.R.; WHITE, J.O.; HORTON, I.M.; PERKINS, D.H.; STRECKFUSS, J.L.; and DREIZEN, S. (1981): Effects of a Single Application of Sodium Fluoride Gel on Dental Plaque Acidogenesis, J Dent Res 60:13961402. BRUUN, C.; GIVSKOV, H.; and THYLSTRUP, A. (1987): Intraoral Hydrolysis of Monofluorophosphate, Scand J Dent Res 95:202-204. CAREY, C.; GREGORY, T.; RUPP, W.; TATEVOSSIAN, A.; and VOGEL, G.L. (1986): The Driving Forces in Human Dental Plaque Fluid for Demineralisation and Remineralisation of Enamel Mineral. In: Factors Relating to Demlneralisatlon and Remlnerallsatlon of the Teeth, S.A. Leach, Ed., Oxford: IRL Press Ltd., pp. 163-173. CAREY, C.; TATEVOSSIAN, A.; and VOGEL, G.L. (1989): Fluoride Concentrations in Overnight-fasted Plaque Fluid from Single Tooth Surfaces, Caries Res (submitted). CHARLTON, G.; BLAINEY, B.; and SCHAMSCHULA, R.G. (1974): Associations Between Dental Plaque and Fluoride in Human Surface Enamel, Arch Oral Bioi 19:139-143. DAWES, C. and JENKINS, G.N. (1962): Some Inorganic Constituents of Dental Plaque and their Relationship to Early Calculus Formation and Caries, Arch Oral Bioi 7:161-172. DAWES, C.; JENKINS, G.N.; HARDWICK, J.L.; and LEACH, S.A. (1965): The Relation between the Fluoride Concentrations in the Dental Plaque and in Drinking Water, Br Dent J 119:164-167. DODDS, M.W.J. and EDGAR, W.M. (1988): The Relationship Between Plaque pH, Plaque Acid Anion Profiles, and Oral Carbohydrate Retention After Ingestion of Several 'Reference Foods' by Human Subjects, J Dent Res 67:861-865. DUCKWORTH, R.M.; MORGAN, S.N.; and MURRAY, A.M. (1987): Fluoride in Saliva and Plaque Following Use of Fluoride-containing Mouthwashes, J Dent Res 66:1730-1734. EDGAR, W.M. (1981): Fluoride Metabolism in Dental Plaque, Bacteria and
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tribution and Metabolic Effects of Human Plaque Fluorine, Arch Oral Bioi 14:105-119. JOHANSEN, E.; TAVES, D.R.; and OLSEN, T.O., Eds. (1979): Continuing Evaluation of the Use of Fluorides. AAAS Selected Symposium, Boulder: Westview Press, pp. 1-110. KASHKET, S. and BUNICK, F.J. (1978): Binding of Fluoride in Oral Streptococci, Arch Oral Bioi 23:993-996. KASHKET, S.; RODRIGUEZ, M.; and BUNICK, F.J. (1977): Inhibition of Glucose Utilization in Oral Streptococci by Low Concentrations of Fluoride, Caries Res 11:301-307. KLIMEK, J.; HELLWIG, E.; and AHRENS, G. (1983): Movement of Fluoride under Cariogenic Conditions, Caries Res 17:315-320. LEVERETT, D.H.; McHUGH, W.D.; and JENSEN, O.E. (1984): Effect of Daily Rinsing with Stannous Fluoride on Plaque and Gingivitis: Final Report, J Dent Res 63:1083-1086. MacFADYEN, E.E.; HILDITCH, T.E.; STEPHEN, K.W.; HORTON, P.W.; and CAMPBELL, J.R. (1979): Distribution of Fluoride in Gingival Fluid and Dental Plaque of Dogs, Arch Oral Bioi 24:427-43l. MAIN, C.; GEDDES, D.A.M.; McNEE, G.S.; COLLINS, W.J.N.; SMITH, D.C.; and WEETMAN, D.A. (1984): Instrumentation for Measurement of Dental Plaque Thickness in situ, J Biomed Eng 6:151-154. McNEE, S.G.; GEDDES, D.A.M.; MAIN, C.; and GILLESPIE, F.C. (1980): Measurements of the Diffusion Coefficient of NaF in Human Dental Plaque in vitro, Arch Oral Bioi 25:819-824. MOODY, G.J. and THOMAS, J.D.R. (1971): Selective Ion Sensitive Elec· trodes, Watford: Merrow Publishing Co. Ltd., p. 66. NOBRE dos SANTOS, M. and CURY, J.A. (1988): Dental Plaque Fluoride is Lower After Discontinuation of Water Fluoridation, Caries Res 22:316317. 6GAARD, B.; GAFFAR, A.; BAHL, M.K.; R6LLA, G.; and HELGELAND, K. (1985): Fluoride Retention in Clean and Plaque-covered Demineralized Enamel in vivo after Application of Monofluorophosphate, Scand J Dent Res 93:486-493. OPHAUG, R.H.; JENKINS, G.N.; SINGER, L.; and KREBSBACH, P.H. (1987): Acid Diffusion Analysis of Different Forms of Fluoride in Human Dental Plaque, Arch Oral Bioi 32:459-46l. OPPERMANN, R.V. and JOHANSEN, J.R. (1980): Effect of Fluoride and Non-Fluoride Salts of Copper, Silver and Tin on the Acidogenicity of Dental Plaque in vivo, Scand J Dent Res 88:476-480. PEARCE, E.I.F. (1981): The Artificial Mineralization of Dental Plaque. In: The Environment of the Teeth, D.B. Ferguson, Ed., Frontiers of Oral Physiology, Vol. 3, Basel: S. Karger, pp. 108-124. PEARCE, E.I.F. (1984): Therapeutic Modifications to the Mineral Ion Composition of Dental Plaque, Caries Res 18:103-110. PEARCE, E.I.F.; HANCOCK, E.M.; and GALLAGHER, I.H.C. (1984): The Effect of Fluorhydroxyapatite in Experimental Human Dental Plaque on its pH, Acid Production and Soluble Calcium, Phosphate and Fluoride Levels Following Glucose Challenge, Arch Oral Bioi 29:521-527. RIPA, L.W. (1984): Need for Prior Tooth Cleaning when Performing a Professional Topical Fluoride Application: Review and Recommendations for Change, JAm Dent Assoc 109:281-285. R6LLA, G. and MELSEN, B. (1975): Desorption of Protein and Bacteria from Hydroxyapatite by Fluoride and Monofluorophosphate, Caries Res 9:66-75. R6LLA, G. and 6GAARD, B. (1986): Studies on the Solubility of Calcium Fluoride in Human Saliva. In: Factors Relating to Demineralisation and Remineralisation of the Teeth, S.A. Leach, Ed., Oxford: IRL Press Ltd., pp.45-50. RUGG-GUNN, A.; EDGAR, W.M.; COCKBURN, M.A.; and JENKINS, G.N. (1981): Correlations Between Fluoride Concentration, Sample Weight and Acid Production in Dental Plaque from Children, Arch Oral Bioi 26:6163. SCHAMSCHULA, R.G.; ADKINS, B.L.; BARMES, D.E.; CHARLTON, G.; and DAVEY, B.G. (1977): Caries Experience and the Mineral Content of Plaque in a Primitive Population in New Guinea, J Dent Res 56 (Spec Iss C): C62-e70. SCHAMSCHULA, R.G.; ADKINS, B.L.; BARMES, D.E.; CHARLTON, G.; and DAVEY, B.G. (1978): WHO Study of Dental Caries Etiology in Papua New Guinea, Geneva: WHO Publication No. 40.
SCHNEIDER, P. and MUHLEMANN, H.R. (1974): The Antiglycolytic Action of Amine Fluoride on Dental Plaque, Helv Odontol Acta 18:63-70. SHERN, R.J. (1988): Effects of Various Organic Compounds and Fluoride on Dental Plaque and Caries in Rats, Caries Res 22:181-186. SHERN, R.; SWING, K.W.; and CRAWFORD, J.J. (1970): Prevention of Plaque Formation by Organic Fluorides, J Oral Med 25:93-97. SHIELDS, W.F. and MUHLEMANN, H.R. (1975): Simultaneous pH and Fluoride Telemetry from the Oral Cavity, Helv Odontol Acta 19:18-26. SINGER, L. and ARMSTRONG, W.D. (1965): Determination of Fluoride, Anal Biochem 10:495-500. SINGER, L.; JARVEY, B.A.; VENKATESWARLU, P.; and ARMSTRONG, W.D. (1970): Fluoride in Plaque, J Dent Res 49:455. STILES, H.M.; BOWEN, W.H.; WITTIG, A.B.; and BRUNELLE, J.A. (1979): Plaque Fluoride Concentration and Caries Prevalence in 12-18 Year-old Children, lADR Prog & Abst 58:No. 1343. SVANBERG, M. and WESTERGREN, G. (1983): Effect of SnF2 Administration as Mouthrinses or Topically Applied on Strep. mutans, Strep. sanguis and Lactobacilli in Dental Plaque, Scand J Dent Res 91:123-129. SVATUN, B. and ATTRAMADAL, A. (1978): The Effect of Stannous Fluoride on Human Plaque Acidogenicity in situ (Stephan Curve), Acta Odontol Scand 36:211-218. TATEVOSSIAN, A. (1978): Distribution and Kinetics of Fluoride Ions in the Free Aqueous and Residual Phases of Human Dental Plaque, Arch Oral Bioi 23:893-898. TATEVOSSIAN, A. (1980): Fluoride and Magnesium in Dental Plaque, Proc Finn Dent Soc 76:103-110. TATEVOSSIAN, A. and GOULD, C.T. (1976): The Compositionof the Aqueous Phase in Human Dental Plaque, Arch Oral Bioi 21:319-323. TAVES, D.R. and GUY, S. (1979): Distribution of Fluoride among Body Compartments. In: Continuing Evaluation of the Use of Fluorides, E. Johansen, D.R. Taves, and T.O. Olsen, Eds., AAAS Selected Symposium, Boulder: Westview Press, pp. 159-185. THIRADILOK, S. and FEAGIN, F. (1978): Effects of Magnesium and Fluoride on Acid Resistance of Remineralized Enamel, Ala J Med Sci 15:144148. TINANOFF, N. and WEEKS, D.B. (1979): Current Status of SnF2 as an Antiplaque Agent, Pediat Dent 1:199-203. TURTOLA, L.O. (1977): Fluoride Content of Dental Plaque Before, During and After Ingestion of Sucrose modified with Fluoride or BicarbonatePhosphate, Scand J Dent Res 85:380-386. TURTOLA, L.O. and LUOMA, H. (1972): Plaque pH in Caries-active and -inactive Subjects Modified by Sucrose and Fluoride, with and without Bicarbonate Phosphate, Scand J Dent Res 80:334-343. WEATHER ELL, LA.; DEUTSCH, D.; ROBINSON, C.; and HALLSWORTH, A.S. (1977): Assimilation of Fluoride by Enamel Throughout the Life of the Tooth, Caries Res 11 (Suppl. 1):85-115. WEATHERELL, J.A.; ROBINSON, C.; and HALLSWORTH, A.S. (1972): Changes in the Fluoride Concentration of the Labial Enamel Surface with Age, Caries Res 6:312-324. WEATHERELL, J.A.; STRONG, M.; RALPH, J.P.; and ROBINSON, C. (1988): Availability of Fluoride at Different Sites in the Buccal Sulcus, Caries Res 22:129-133. WEATHERELL, J.A.; STRONG, M.; ROBINSON, C.; and RALPH, J.P. (1986): Fluoride Distribution in the Mouth after Fluoride Rinsing, Caries Res 20:111-119. WHITFORD, G.M.; PASHLEY, D.H.; and PEARSON, D.E. (1981): Fluoride in Gingival Crevicular Fluid and a New Method for Evaporative Water Loss Correction, Caries Res 15:399-405. WHITFORD, G.M.; SCHUSTER, G.S.; PASHLEY, D.H.; and VENKATESWARLU, P. (1977): Fluoride Uptake by Streptococcus mutans 6715, Infect Immun 18:680-687. WILSON, R.F. and ASHLEY, F.P. (1988): Collection and Biochemical Analysis of Human Dental Plaque from the Approximal Tooth Surfaces and Comparison with Plaque from Free Smooth Surfaces, Arch Oral Bioi 33:473478. WOOLLEY, L.H. and RICKLES, N.H. (1971): Inhibition of Acidogenesis in Human Dental Plaque in situ Following the Use of Topical Sodium Fluoride, Arch Oral Bioi 16:1187-1194.
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J Dent Res 69(Spec Iss):645-652, February, 1990
Introduction. Research has continued to seek answers to some of the questions raised in the previous Workshop on Cariostatic Mechanisms of Fluorides (Jenkins and Edgar, 1977). Reviews have appraised some of these questions (Tatevossian, 1980; Edgar, 1981; Geddes and Rolla, 1988), and some of the material therein is included in this presentation where appropriate.
in F concentration. Theoretically, the detection limit is determined by the solubility of the europium-doped lanthanum fluoride crystal, but estimates of the solubility product have ranged from 3.3 X 10- 25 to 7 X 10- 17 (Moody and Thomas, 1971). In practice, the detection limit for F is close to 1 umol/L (0.019 ppm F), and most commercial electrodes show both a nonlinearity in Nernstian response in the range below 5 urnol/L (0.095 ppm F) as well as considerable slowing in electrode 99% response time in this range. Birkeland and Speirs (1977) pointed out that despite the improved method of measuring fluoride ion, analyses of dental plaque have often been carried out at the limit of sensitivity of the electrode and without giving calibration data at this analytically marginal level. This still seems to be the case when average F concentrations of reaction mixtures measured with the electrode are calculated from the literature (Table 2). The data in Table 1 should be evaluated by reference to Table 2 where possible. Some of the data (Table 1) are based on analyses close to or below the detection limit of the electrode (Table 2) and should be considered approximate rather than absolute. It is thus not prudent to give a definitive value for plaque F, although most estimates of plaque total F are in the range 5-10 mg F/kg wet weight (or ppm F). Comparatively higher values are found in plaque from subjects receiving fluoridated water (Table 1), including the few reports on plaque fluid F. Isotachophoresis and ion chromatography are at about the same level of sensitivity as the F electrode and to date have not been exploited to any significant extent (Geddes and Rolla, 1988). Analytical problems have also beset the reliable description of the compartments of F in plaque. Until recently, most workers believed that total plaque F could only be obtained after digestion in hot acid (Jenkins and Edgar, 1977; Edgar, 1981; Geddes and Rolla, 1988). Ophaug et at. (1987) confirmed an earlier report by Gaugler and Bruton (1982) that cold perchloric acid removed >95% of plaque total F (Table 1), and it may now be unsound to distinguish between plaque F compartments on the basis of their extraction by different reagents and conditions. The implications of this finding are discussed in more detail below.
Sources of plaque fluoride. Analytical considerations. The use of the fluoride electrode in the late 1960's heralded a significant advance over earlier colorimetric methods for fluoride analysis in dental plaque (Singer and Armstrong, 1965; Gren et al., 1969). Most F-electrode estimates of the total fluoride concentration in plaque tend to be 2-5 times lower than those from colorimetric assays (Table 1). The potentiometric F analysis implies an order of magnitude increase in sensitivity with each order of magnitude decrease Presented at a Joint IADR/ORCA International Symposium on Fluorides: Mechanisms of Action and Recommendations for Use, held March 21-24, 1989, Callaway Gardens Conference Center, Pine Mountain, Georgia
Jenkins and Edgar (1977) reviewed this topic and concluded that the diet and saliva, but not enamel, are sources of plaque fluoride. Usually, enamel is unlikely to be a source for plaque F, and the reverse has been proposed (Charlton et al., 1974), especially on cervical enamel surfaces habitually covered by plaque (and possibly demineralized by plaque) where F is higher (Weatherell et al., 1972, 1977). Were enamel F the usual source for plaque F, regular toothbrushing with F-free toothpaste, as in the data of Weatherell et al., would have depleted F in cervical enamel. The reverse was found to be the case. However, under demineralizing conditions, it is possible to demonstrate an in vitro uptake of fluoride from enamel by thick films of Streptococcus mutans FA1 (Klimek et al., 1983). However, this could not occur repeatedly without depleting enamel fluoride, which has not been found to be the case on 645
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TABLE 1 SOME ESTIMATES OF FLUORIDE IN DENTALPLAQUE(Mean ± SD)
Wet (W) or dry (D) weight basis
Low
Pre-electrode (mglkg) Hardwick & Leach (1962) D W Dawes et al. (1965) Post-electrode Plaque fluid F (}JJ1lol/L) Edgar & Tatevossian (1971) Hassell et aI. (1971) Shields & Muhlemann (1975) Tatevossian & Gould (1976) Tatevossian (1978) Carey et aI. (1986) Bound F (mgfkg wet [Wi or dry [D] weight) from cold acid extracts Gren et al. (1969) W D Brown et al. (1981) W W Gaugler & Bruton (1982) Geddes & McNee (1982) W W Grobler et aI. (1982) W Brown et aI. (1983) D Pearce (1984) Duckworth et aI. (1987) W W Ophaug et al. (1987) D Nobre dos Santos & Cury (1988) Total F (mg/kg wet [Wi or dry [D] weight) from hot acid digests Singer et al. (1970) W D Birkeland et al. (1971) D Agus et al. (1976) Schamschula et aI. (1977) D W Turtola (1977) D Tatevossian (1978) W Agus et aI. (1980) Rugg-Gunn et aI. (1981) W W Geddes & McNee (1982) W Gaugler & Bruton (1982) W Ophaug et al. (1987) D Wilson & Ashley (1988) D
-100 umol/L (-2 ppm) 235 47 :!: 22
125 25 ± 17 -29 12 (wet) 3.3 (dry)
Pearce (1984) Duckworth et al. (1987) Ophaug et al, (1987) Nobre dos Santos & Cury (1988)
in in in in in in in in
Average F Concentration (urnol/L) in Analyzates
1.5 mL 1.2 mL 0.4 mL 0.1 mL 1 mL 0.2 mL 1 mL 1 mL
in 1 mL in 1 mL in 1 mL in 1.3 mL in 0.2 mL in 1 mL in 1 mL
2.9 0.7 (low F) 1.4 (high F) 1.3 3.3 38.6 12.7 1.5 5.1
2.5 0.6 (low F) 1.6 (high F) 0.7 1.0 '70.1 0.3 52.6 > 1.1 3.8
'Mineralized plaque.
(> 95%) by cold 0.5 mol/L perchloric acid, and since the ionized F in plaque fluid constitutes 10 times the concentrations reported in plaque fluid (Table 1). There is a lack of data on the F concentrations in plaque fluid during sugar fermentation. Turtola (1977) calculated from plaque extracts that ionized F may rise to - 50 umol/L in plaque during daily ingestion of 10 x 2 g tablets of sucrose. If the entire plaque F (- 5 mglkg wet weight; Table 1) were released during fermentation, the F concentration in plaque fluid is unlikely to exceed 1 mmol/L, and the rapid decline of soluble F in plaque (see below) implies that bacterial inhibition would be too short-lived even in these circumstances.
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TATEVOSSlAN
Can plaque F concentrations approach those for currently proposed mechanisms of action of plaque F? Although the therapeutic action of fluoride in reducing the incidence of dental caries has been considered to depend on a multiplicity of effects on the enamel and dental plaque, demonstrations of some of these effects have spanned several orders of magnitude in fluoride concentration (Table 4, based on Tatevossian, 1980). Plaque appears not to reduceenamel uptakeof F from rinses (review by Ripa, 1984), although MFP uptake is enhanced, presumably by enzymatic hydrolysis in dentalplaque(Jackson, 1982; Ogaard et al., 1985; Hellwig et al., 1987; Briiun et al., 1987). The reduction in plaque deposits by stannous or aminefluoride either in rinses or toothpaste is a clinically significant effect at - 5 mmol/L (Table 4), albeit being based on the cation rather than on the Fanion (Tinanoff and Weeks, 1979; Shern et al., 1970). Surprisingly, stannous fluoride has no demonstrable anti-plaque effect after 16 months' continuous use as a mouthrinse (Leverett et al., 1984) and may cause a rise in salivarylactobacillus counts(Svanberg and Westergren, 1983). Whether bound F inhibits plaque metabolism remains questionable, as does the possibility that such effects are exhibited by F released during fermentation. In plaque not containing native or introduced mineral, such release appears unlikely to achieve concentrations of F in plaque fluid for periods of time sufficient to inhibit bacterial metabolism, or indeed to achieve most of the effects proposed for plaque F (Table 4), exceptfor enamel remineralization and a reduced solubility rate for enamel hydroxyapatite.
Can bound F be increased in dental plaque by topical means in order to reach therapeutically significant levels? The kinetics of soluble inorganic F in dental plaque is too rapid to allow a significant build-up of F using conventional rinses(Table 5). In the studyby Birkeland et al. (1971),plaque F was abovebaselinevalues 24 h after a rinsewith NaF (Table 5), which is contraryto the general trend of other studies (Table 5). However, the plaqueweightsfor four-hour and 24-hour samples were lower than those of the 2-4-day samples (thus tending to give higher F values), while the five-day samples, which were as low in average weight as the 24-hour samples, also demonstrated high F values. Even though these were not statistically above the baseline values, they were in the same range as the 24-hour data (which were statistically above baseline values). These authors noted that, with increasing weight of deposits, the F concentrations decreased. Moreover, the
average dry weights of all their samples (see Table 2) were low, in the range 1.12 mg (four-hour samples) to 1.67 mg (three-day sample). Hassell et al. (1971) ascribed the rapid kinetics of free F in plaque (Table 5) to bindingwithinplaque but gave no evidence to substantiate this conclusion. In four- or five-day control plaque, F activity was as high as 100 urnol/L or greater (Shields and Miihlemann, 1975). These data suggest the need for caution in the interpretation of telemetric data. Single daily mouthrinses over a period of four weeks were reported to cause small increases of bound F in plaque collected > 18 h after the last application (Duckworth et al., 1987; Table 5). The range of plaque bound F was low, however 1.2 ppm in controls, and 3.3 ppm four weeks after use of 0.053 mol/L F (Table 1) - and their analyzate concentrations were on average below the detection limit for the F electrode (Table 2). A marked fall in plaque boundF following cessation of fluoridation was reported in Brazilby Nobredos Santosand Cury (1988). However, their post-fluoridation values (Table 1) are the lowestyet reported in dental plaque (1.7 :+: 0.6 SD mg/kg dry weight). In contrast to the modest and short-lived effects of soluble fluoride (Table 5), therapeutically significant levelsof fluoride as well as calcium and phosphate were shown to be retained > 16 h in dental plaque following rinses (four times daily) with a mouthrinsecontaining urea, calcium,phosphate, and fluoride (Pearce, 1984; Table 5). Pearce et al. (1984) showed that loading plaquewith mineral could lower its acidogenicity (Table 3) and reduceits softening effecton bovine enamel in vitro. Clinical trials are needed to evaluate the caries-preventive efficacy of this formulation. We have much yet to learn about the dynamics of fluoride in dental plaque at different sites in the mouth under fluctuating intra-oral conditions.
Implications for the rational use of fluorides. Cationic fluoride preparations containing metal ions are effective in the short term in reducing plaque formation (Table 4). The presence of plaque during topical treatments may be advantageous and is not detrimental to the efficacy of fluoride uptake by enamel or F effects on mineral turnover. Fluoridationof the waterseems to be a mechanism for increasing plaque F. The evidence for the effect of fluoride, as distinct from metal ions, in inhibiting plaque metabolism is far from being conclusive and, at most, suggests that a smalleffect is possible for short periods after pulsing plaque with high F concentrations. There are prospects for developing fluoride preparations which can be retained in dental plaque at therapeutic concentrations for sufficiently long to be beneficial. REFERENCES AGUS, H.M.; UN, P.S.H.; COOPER, M.H.; and SCHAMSCHULA, R.G. (1980): Ionized and Bound Fluoride in Resting and Fermenting Dental
TABLE 4 FLUORIDEEFFECfS DEMONSTRATED AT DIFFERENT CONCENTRATIONS Concentration (mol/L) 0.5
5 X 10- 3 1 X 10- 3 5 X 10-' 5 X 10-s 5 X 10- 6
Effect Desorptionof bacteria from apatite Reduction in plaque formation Desorption of albumin from apatite Inhibition of bacterial metabolism Fluoridation reduces dental caries and may affect fissure morphology Reduces solubility rate of apatite Enhances remineralization of apatite
Reference Rolla & Melsen, 1975 Tinanoff and Weeks, 1979 Rolla & Melsen, 1975 Hamilton, 1977 Johansen et al., 1979 Thiradilok & Feagin, 1978
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Vo!. 69 SpeciaZ Issue
PLAQUE FLUORIDE
651
TABLE 5 KINETICS OF FLUORIDE IN DENTAL PLAQUE Concentration
Duration of Elevated Plaque F
(rnol/L) 0.05 NaF 0.05 NaF 0.05 NaF weekly 0.05 NaF 0.05 NaF Not Known
0.02 NaF 5-26 X 10- 5 NaF in milk 0.048 NaF 0.005,0.013 or 0.053 NaF daily for 4 weeks 0.005 MFP + NaF 4 x daily rinse with mineralizing solution
Reference
60% above baseline 24 h later mostly eliminated within 1 h 2 x above baseline after 1 day 1 h (4- or 7-day plaque) No elevation during eating 2 g sucrose + 50 or 20 ug F as NaF 16 h
Pearce, 1984
Plaque and Individual Human Caries Experience, Arch Oral Bioi 25:517522. AGUS, H.M.; SCHAMSCHULA, R.G.; BARMES, D.E.; and BUNZEL, M. (1976): Associations Between the Total Fluoride Content of Dental Plaque and Individual Caries Experience in Australian Children, Community Dent Oral Epidemiol 4:210-214. BIRKELAND, J.A. (1970): Direct Potentiometric Determination of Fluoride in Soft Tooth Deposits, Caries Res 4:243-255. BIRKELAND, J.M. and CHARLTON, G. (1976): Effect of pH on the Fluoride Ion Activity of Plaque, Caries Res 10:72-80. BIRKELAND, J.M.; JORKJEND, L.; and VON DER FEHR, F.R. (1971): The Influence of Fluoride Rinses on the Fluoride Content of Dental Plaque in Children, Caries Res 5:169-179. BIRKELAND, J.M. and ROLLA, G. (1972): In vitro Affinity of Fluoride to Proteins, Dextrans, Bacteria and Salivary Components, Arch Oral Bioi 17:455-463. BIRKELAND, J.M. and SPEIRS, R.L. (1977): Discussion, Caries Res 11 (Suppl. 1):237-242. BROWN, L.R.; WHITE, 1.0.; HORTON, I.M.; DREIZEN, S.; and STRECKFUSS, J.L. (1983): Effect of Continuous Fluoride Gel Use on Plaque Fluoride Retention and Microbial Activity,J Dent Res 62:746-751. BROWN, L.R.; WHITE, J.O.; HORTON, I.M.; PERKINS, D.H.; STRECKFUSS, J.L.; and DREIZEN, S. (1981): Effects of a Single Application of Sodium Fluoride Gel on Dental Plaque Acidogenesis, J Dent Res 60:13961402. BRUUN, C.; GIVSKOV, H.; and THYLSTRUP, A. (1987): Intraoral Hydrolysis of Monofluorophosphate, Scand J Dent Res 95:202-204. CAREY, C.; GREGORY, T.; RUPP, W.; TATEVOSSIAN, A.; and VOGEL, G.L. (1986): The Driving Forces in Human Dental Plaque Fluid for Demineralisation and Remineralisation of Enamel Mineral. In: Factors Relating to Demlneralisatlon and Remlnerallsatlon of the Teeth, S.A. Leach, Ed., Oxford: IRL Press Ltd., pp. 163-173. CAREY, C.; TATEVOSSIAN, A.; and VOGEL, G.L. (1989): Fluoride Concentrations in Overnight-fasted Plaque Fluid from Single Tooth Surfaces, Caries Res (submitted). CHARLTON, G.; BLAINEY, B.; and SCHAMSCHULA, R.G. (1974): Associations Between Dental Plaque and Fluoride in Human Surface Enamel, Arch Oral Bioi 19:139-143. DAWES, C. and JENKINS, G.N. (1962): Some Inorganic Constituents of Dental Plaque and their Relationship to Early Calculus Formation and Caries, Arch Oral Bioi 7:161-172. DAWES, C.; JENKINS, G.N.; HARDWICK, J.L.; and LEACH, S.A. (1965): The Relation between the Fluoride Concentrations in the Dental Plaque and in Drinking Water, Br Dent J 119:164-167. DODDS, M.W.J. and EDGAR, W.M. (1988): The Relationship Between Plaque pH, Plaque Acid Anion Profiles, and Oral Carbohydrate Retention After Ingestion of Several 'Reference Foods' by Human Subjects, J Dent Res 67:861-865. DUCKWORTH, R.M.; MORGAN, S.N.; and MURRAY, A.M. (1987): Fluoride in Saliva and Plaque Following Use of Fluoride-containing Mouthwashes, J Dent Res 66:1730-1734. EDGAR, W.M. (1981): Fluoride Metabolism in Dental Plaque, Bacteria and
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