MODE OF ACTION OF FLUORIDE: APPLICATION OF NEW TECHNIQUES AND TEST METHODS TO THE EXAMINATION OF THE MECHANISM OF ACTION OF TOPICAL FLUORIDE

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1 MODE OF ACTION OF FLUORIDE: APPLICATION OF NEW TECHNIQUES AND TEST METHODS TO THE EXAMINATION OF THE MECHANISM OF ACTION OF TOPICAL FLUORIDE DJ. WHITE D.G.A. NELSON R.V. FALLER The Procter & Gamble Company Health Care Division Grooms Road Cincinnati, Ohio Adv Dent Res 8(2): , July, 1994 Abstract Modern techniques in dental research continue to assist in the study of the mode of (anticaries) action of topical fluorides. The Plaque Glycolysis and Regrowth Model (PGRM) facilitates the standardized assessments of antimicrobial effects on plaque following use of test formulations in vivo without complications arising from coincident mineral reactivity. In vivo plaque glycolysis testing demonstrates that topically applied fluoride, at conventional levels found in dentifrices, has only modest effects on the metabolic (acid-producing) activity of dental plaque. Any 'plaque' contribution to fluoride efficacy must come from more subtle effects on plaque acidogenicity than those measured in PGRM. The 19-F MAS NMR (Magic Angle Spinning Nuclear Magnetic Resonance) technique provides unambiguous measures of the reaction products of F-enamel interactions. Studies have revealed a new 'reaction product' of fluoride-enamel interactions designated as Non-Specifically-Adsorbed Fluoride, NSAF. This species, along with FAP (fluoroapatite), FHAP (fluorohydroxyapatite), and CaF 2 (calcium fluoride), contributes to the remineralization/ demineralization benefits of fluoride. ph cycling and in situ denture chip studies permit quantitative assessments to be made of the relative benefits of fluoride in promoting remineralization and in inhibiting demineralization. Results from ph cycling/m situ experiments are strongly supportive of Koulourides' 'Acquired Acid Resistance' concept, describing fluoride's decay-preventive effects. The continued application of new analytical/physical techniques and testing regimens to the study of fluoride anticaries mechanisms may lead to the development of improved fluoride agents/treatment modalities for the prevention of dental caries. This manuscript was presented at a Symposium entitled "Mechanisms and Agents in Preventive Dentistry", held October 28-November 1, 1992, in Chester, England, under the auspices of the Council of Europe Research Group on Surface and Colloid Phenomena. T he development of improved fluoride agents and formulations remains an important goal of researchers, clinicians, and dental product manufacturers. The attainment of this goal demands an improved understanding of the mechanism of action of fluoride in preventing tooth decay. Although the anticaries effectiveness of fluoride has been known for over five decades, some debate still surrounds the dominant 'mode of action' {i.e., anticaries mechanisms) of fluoride. Central to this debate is research devoted to: - a quantitative determination of the relative importance of fluoride's effects on dental plaque vs. tooth mineral; - a better understanding of the influence of different fluorideenamel reaction products on caries progression/reversal; and - the elucidation of the relative importance of remineralization enhancement and demineralization protection to fluoride's anticaries effects. In the last decade, numerous advances have been made in analytical/physical techniques and testing regimens for assessing fluoride effects on caries processes. In our laboratory, we have developed and applied new techniques related to all three of the reaction modes of fluoride highlighted above. This includes a Plaque Glycolysis and Regrowth method capable of assessing the effects of antimicrobials on plaque metabolic activity in situ\ a Magic Angle Spinning NMR method capable of assessing fluoride reaction products formed on the surfaces of enamel crystals; and ph cycling in vitro and in situ protocols capable of assessing the net effects of fluoride on enamel mineral flux under countercurrent conditions of de- and remineralization associated with caries development/ prevention. This paper describes our application of some of these techniques and methodologies to the research topics outlined above. MATERIALS AND METHODS PGRM Assessments of Fluoride Effects on Plaque Glycolysis In the PGRM experiment, 16 healthy subjects were asked to refrain from toothbrushing overnight and presented in the morning without eating or drinking (except for water). The subjects were regular users of fluoridated dentifrices. A plaque sample was removed from the buccal and lingual surfaces of teeth in the mandibular left quadrant (by sterile cotton swabbing along the gingival margin and between teeth) and stored in a 166

2 VOL. 8(2) MODE OF ANTICARIES ACTION OF FLUORIDE 167 TABLE 1 SURFACE HARDNESS, FLUORIDE UPTAKE, AND MICRORADIOGRAPHY CHANGES DURING ph CYCLING Dentifrice Placebo NaF VHN i ] AND ACQUIRED (SECONDARY) ACID RESISTANCE (AAR) TESTING VHN 89.7D VHN aar 2i. in 52.3 n AD AD -9.6 n -o.9 n AZ -3024: -719: Lesion Depth 70: 44: Min. Min 91o VHN = Vickers Hardness Number at start of ph cycling (sound enamel = 350). VHN c = Vickers Hardness Number post-ph-cycling. VHN aar = Vickers Hardness Number following secondary acid exposure. AD c = Linearized Surface Hardness change following cycling. AD aar = Linearized Surface Hardness change following secondary acid exposure. AZ aar = Microradiography AZ change following secondary acid exposure. ~ Lesion Depth = um lesion depth following secondary acid exposure. ~ Min Mineral % = Volume % mineral minimum found in lesions following secondary acid exposure. F c = Fluoride uptake ( ig per sq. cm) measured post-cycling. F aar = Fluoride uptake measured post-secondary acid exposure. Means outside brackets are statistically different at p < 0.05 (ANOVA). (From White, 1991) 30: 72: F 13.95: ns ns F 15.62: sealed sterilized vial at 0 C. This plaque sample served as a baseline control for subsequent samples following treatment. Subjects were asked to brush their teeth with 2.5 g of designated test dentifrice for 30 s with instructions to brush only the baseline sampled area {e.g., the mandibular left quadrant). Subjects were asked to swish dentifrice slurry for an additional 30 s throughout their dentition prior to expectorating. (For mouthrinsing, subjects were asked simply to swish with neat mouthrinse for a full 30 s.) Following use of the test agent (rinse or paste), subjects were asked to collect plaque samples from remaining quadrants (LL, LR, UR) in sequence at 15,45, and 90 min post-treatment. Plaque swabs were vortexed into 1.75 ml of 0.03% TSB broth (ph 7.30). Aliquots of this suspension were serially diluted to 0.20 OD 600 nm in a spectrophotometer to standardize samples for biomass. Onemilliliter aliquots of standardized plaque were inoculated with 0.05 ml of 40% sucrose in an Eppendorf vial and were placed on an Eppendorf thermomixer (type 5436) for incubation under vigorous agitation at 37 C. The ph drop over 2 h of incubation was recorded (by ph electrode) as a measure of standardized plaque glycolytic activity. Subjects participated in PGRM tests only once/week to avoid carryover and contamination potential. 19F MAS NMR Assessments of Mineral Fluoridation Lesion biopsy preparation/artificial and natural white spots The initial reaction products of fluoride with caries enamel were obtained from the collection of mineral from artificial white-spot lesions from a ph-cycling remineralization study (Wietfeldt et al, 1988), the protocol of which is briefly described in the next section. Following analysis for fluoride content and remineralization, lesion mineral was collected by multiple biopsies of the treated enamel and pooled for NMR analysis. For the assay of 'mature' fluoride-enamel reaction products, biopsies of incipient lesions were carried out in extracted molars and pre-molars obtained from local periodontists. Teeth were stored in buffered formaldehyde solution (ph = 7) prior to analysis and were assayed less than 3 months following extraction. Incipient lesions were identified on interproximal surfaces visually by air-drying. Treatment of powdered enamel Powdered enamel was treated with supernatant liquids of 25% water dentifrice slurries, facilitating a direct look at the initial reaction products of enamel with topical fluoride dentifrice (not having undergone any periods of de- or remineralization.) NMR 19-F MAS NMR spectra were obtained on a Bruker CXP-300 spectrometer equipped with a standard 5-mm ultrafast spinning probe from Doty Scientific, as described in detail by Kreinbrink et al. (1990). Fluorine chemical shifts are referenced to C 6 F 6 standard. ph Cycling Assessments of AAR Contribution to Caries Prevention In the ph-cycling experiments, artificial carious lesions were initially prepared (White, 1988a) and exposed to countercurrent conditions of de- and remineralization (White, 1987, 1988b). Saliva served as the remineralization fluid, and toothbrushing/ dentifrice exposure was simulated by four one-minute immersions of artificial lesions in 25% water slurries of dentifrice daily. Remineralization was assessed by linearized changes in surface microhardness (AD in Table 1; see White, 1987,1988a,b) along with microradiography, and lesions were also assayed for fluoride uptake. At the conclusion of ph cycling, following hardness and F-uptake analysis, lesions

3 168 WHITE ETAL ADV DEW RES JULY1994 FAP CaF, FAP/CaF, Solid Mix Time After Brushing (minutes) - A - Peridex - - Crest AFC Fig. 1 Comparison of plaque glycolysis (acid production) following toothbrushing with NaF dentifrice or mouthrinsing with 0.12% chlorhexidine. Individual quadrants sampled at 15, 45, and 90 min post-treatment. ph is indicative of post-incubation ph of plaque samples dispersed in sucrose media (initial ph measured 7.1 for all samples). Treatment effects can be assessed relative to the 0 time baseline (untreated) plaque. were exposed to an extended acid challenge in demineralization media for measurement of acquired resistance to acid decalcification. PGRM Results RESULTS Formulations compared in PGRM testing included a NaF dentifrice (Crest, 0.243% NaF-1100 ppm as F) and a 0.12% chlorhexidine mouthrinse (Peridex ). Results are shown in Fig. 1. Thirty seconds' rinsing with chlorhexidine was observed to eliminate plaque glycolytic activity for the entire 90 min post-treatment. This is consistent with chlorhexidine's strong antimicrobial efficacy and excellent substantivity (Rolla and Melson, 1975). Toothbrushing with a NaF dentifrice, on the other hand, provided only modest antiglycolytic effects within the plaque 15 min post-brushing. This effect dissipated with time and plaque glycolytic activity was not observed to be significantly inhibited (vs. baseline) in samples taken at 45 and 90 min. 19 F MAS NMR Results NMR spectra of various potential calcium-apatite-fluoride mineral salts measured at high (±15.5 khz) spinning speeds are highlighted in Fig. 2. At these high spinning speeds, the solidstate NMR spectra of fluoroapatite, as shown in Fig. 2, are characterized by a narrow resonance at a 64-ppm isotropic chemical shift, whereas CaF 2 is observed to have a (homonuclear dipolar) broadened resonance at 58 ppm. As illustrated in Fig. 2, the high spinning speeds available today facilitate spectral resolution much better than previously observed (White etal., 100 ppm 50 Fig. 2 Fast-spinning solid-state 19-F NMR spectra of fluoroapatite, calcium fluoride, and fluorohydroxy apatite, illustrating the excellent sensitivity of NMR in distinguishing F reaction products with apatites. 1988; Kreinbrink et al, 1990). The spectrum obtained from mature white-spot incipient caries enamel is shown in Fig. 3. This spectrum is indicative of a fluoridated hydroxyapatite FHAP of formula: Ca ]0 (PO 4 ) 6 OHF 2x where the chemical shift varies from ppm, depending upon the extent of substitution x. As x approaches 2, the chemical shift approaches 60 ppm. Overall, we have found that most dental mineral components (mineralized plaque, supragingival calculus, subgingival calculus, sound enamel, sound dentin, etc.) contain large amounts of fluoridated hydroxylapatites, indicating that this is the favored phase to which minerals evolve under intra-oral conditions, as would be predicted from thermodynamic arguments (Driessens, 1982; Brownetal., 1977; Morenos ai, 1977; White and Nancollas, 1990). The solid-state 19-F MAS NMR spectrum of powdered dental enamel treated with NaF dentifrice is shown in Fig. 4. A major absorption occurs at 44-ppm chemical shift not at the 58-ppm shift of calcium fluoride or the 64-ppm resonance expected for fluoroapatite. Research in our laboratories has verified that this resonance is characteristic of non-specificallyadsorbed fluoride (NSAF), as originally proposed by Nelson (Arends et al 1984), shown in Fig. 5. NSAF fluoride is best described as fluoride which is hydrogen-bonded to the phosphate protons on the apatite surface. The fluoride in this form may differ substantially from apatitic-bound F in solution chemical behavior (Arends et al, 1984). The 19-F MAS NMR spectra of mineral collected from artificial carious lesions (as part of a ph-cycling remineralization/demineralization study) are shown in Fig. 6. As shown, lesions treated with NaF exhibited peaks characteristic of both fluorohydroxylapatite and NSAF. [The

4 VOL. 8(2) MODE OFANTICARIES ACTION OF FLUORIDE 169 NSA-F Enamel White Spot I I I 1 I 1 I I I I I I I I I PPM Fig. 3 Fast-spinning solid-state 19-F NMR spectra of powdered enamel collected from mature white-spot areas. Spectrum is directly compared with that offap. The chemical shift is indicative of a highly fluoridated FHAP. PPM Fig. 4 Fast-spinning solid-state 19-F NMR spectra of powdered human dental enamel that has been topically treated with a 25% aqueous slurry of 0.243% NaF dentifrice. Spectrum shows no calcium fluoride resonances only that of a species with an isotropic chemical shift of 44 ppm (NSA-F) and a relatively small FHAP resonance at around 62 ppm. broad resonance downfield of these peaks is an artifact of the NMR technique used with sample sizes this small and can be ignored (Kreinbrink etai, 1990).] The presence of resonances for both FHAP and NS AF suggests the conversion of initially deposited NS AF to FHAP under the periods of cycling de- and remineralization. ph Cyclmg/iw situ Assessments of AAR Results Table 1 highlights results obtained in in vitro ph-cycling comparisons of NaF dentifrices to placebo (non-fluoride) dentifrice (from White, 1991). As shown in Table 1, the artificial lesions treated with NaF dentifrice were observed to harden about two-fold relative to the placebo-treated lesions under ph-cycling conditions (AD changing from 2 to 4 units). Thus, during the cycling phase of the experiment, the lesions actually were reversing (gaining mineral), with the NaFtreated lesions exhibiting increased repair. This remineralization was far from complete, however, since the lesions treated with NaF still exhibited surface hardness some 225 Vickers Hardness Units lower than that of sound enamel. (Complete lesion consolidation would amount to a AD of 7.5 units.) This net remineralization was accompanied by fluoride uptake of 14 ig/cm 2. The test results following extended (secondary) acid challenge are also shown in Table 1. Following the acid exposure, a 10-fold difference in linearized surface hardness was observed between placebo- and NaF-dentifrice-treated lesions. This difference represented 5 times the difference observed during net (ph cycling) remineralization. Microradiographic analysis confirmed the large differences in total mineral content, lesion depth, and lesion minimum mineral content following the acid exposure. Of considerable interest were the fluoride analyses obtained following the acid challenge, which were statistically comparable with the levels observed following the ph-cycling portion of the experiment. We have observed similar phenomena in denture-chip studies where fluoride acquisition occurs in vivo under normal brushing conditions. Table 2 shows the results of such an in situ study, carried out in collaboration with Dr. George Stookey and co-workers at the Indiana University Oral Health Research Institute. Panelists wore appliances specially designed to hold artificial carious lesions for periods of two weeks. Panelists brushed with fluoride (Advanced Formula Crest) or placebo dentifrice in a cross-over design. Following in situ exposure, artificial lesions were assessed for mineral changes and fluoridation by means of the techniques described above. The results showed an enhancement in remineralization, in this case accounting for a change of+177 AZ units, for the fluoridetreated lesions as compared with baseline. (AZ refers to jam x Vol % mineral, the standard measure of caries lesion mineral loss as assessed by microradiography. A positive change in AZ reflects remineralization.) Placebo-treated lesions remineralized about 1/3 as much, with the change in AZ measuring some 50 units. In terms of surface hardness, the effects were similar: 2.3 units' increase for placebo (AD) as compared with 3.0 for the NaF dentifrice. Post-acid challenge results mimicked the pattern we have observed in vitro, with the difference in AZ mineral from microradiography increasing to 300 units and the change in surface hardness measuring some 3.5 (AD) units. Wefel et al. (1989), in a comparison of in situ response of artificial carious lesions in dentin and enamel (with NaF and placebo dentifrices), has generated additional in vivo data in support of the AAR contribution to caries prevention. As shown in Table 3, Wefel etal (1989), in a crown single-section model, observed net remineralization of some +106 AZ units for NaF-treated enamel lesions. This compared with net loss of about -400 AZ units for enamel lesions brushed with placebo. While this difference in mineralization was statistically significant, it was considerably lower in magnitude than the difference observed within the dentin lesions, where NaFtreated lesions decalcified some 4000 AZ units fewer than the placebo controls. These data provide additional support to the

5 170 WHITE ET AL AmlksT Ru JULY 1994 layer \ (calciumrich) I 1 'ca 2 ' Ca 2 ' F- hydrogen bonding -F" H \> \ / \ P va, 2-V P P Ca 2 ' H H o oon /O< p. p. A A enamel crystallites F H5+ 2- I A Ca 2 x Ca! F H H 2- I 2-1 o o A ' X F' AFC FHAP 62.9 ppm ppm ± 2.2 ng/cm 2 Fig. 5 Structure of NSAF fluoride as proposed by Nelson. From Arends et al. (1984). Reproduced with the permission of the publisher, Karger (Basel). importance of AAR, if one considers the fact that dentin mineral is known to be more acid-soluble than enamel mineral, and therefore would be expected to derive greater AAR benefits under caries conditions. DISCUSSION The Relative Importance of 'Antiplaque' Effects to the Anticaries Activity of Topical Fluoride: Studies Applying the PGRM Technique There is a large body of theoretical and experimental evidence suggesting that topical fluoride at high concentrations can provide anticaries effects through specific interactions with dental plaque. Direct effects on plaque bacterial metabolism of carbohydrates could reduce the acid challenge affecting the teeth (Edgar et al., 1970; Geddes and McNee, 1982;Eisenberg et al., 1985; Hamilton and Bowden, 1988; Hamilton, 1990). Frequent application and retention of topical fluoride in plaque could also influence microflora within the mouth, promoting a less cariogenic ecology (Bowden, 1990; Marsh and Bradshaw, 1990; Marquis, 1990). Additional potential anticaries effects of fluoride on plaque could include effects on extracellular polysaccharide formation and effects on bacterial colonization (Hamilton, 1990; Van Loveren, 1990). In general, the clinical contribution of fluoride 'anti-plaque' effects to caries protection is poorly understood, with the supporting evidence (in these authors' opinion) primarily anecdotal. The F-plaque effects are difficult to study, since concomitant reactivity with dental enamel minerals complicates direct assessments of effects on plaque metabolism. In our laboratory, we have attempted to obtain a different perspective on the relative contributions of fluoride 'anti-glycolytic' effects to caries prevention by: (1) separating the plaque/mineral components of reactivity; and (2) comparing treatment effects with those of known antimicrobials like chlorhexidine, by use of the PGRM (White et al., 1993). Dentifrices contain combinations of ingredients which may, in principle, affect bacterial metabolism, including flavor oil components, surfactants, and fluoride. While it is impossible to differentiate among the specific components of the toothpaste Fig. 6 Fast-spinning solid-state 19-F NMR spectra of biopsied enamel from artificial lesions undergoing phcycling remineralization and demineralization with commercial 0.243% NaF dentifrice treatment. AFC refers to Advanced Formula Crest (1100 ppm NaF in silica abrasive). Fluoride uptake found for the sample is shown on the right. Note that the NaF -dentifrice-treated sample exhibited both NSAF and FAP peaks. affecting plaque in this study (these are under study in our laboratories), the general results reported here suggest that topical fluoride from the over-the-counter dentifrices affects only minimal reductions in acute plaque metabolic (acid production) activity. It should be noted that the magnitude of effects observed in these PGRM studies (reductions in twohour minimum ph of the standardized plaques of ph units for min following treatment; see Fig. 1) is not dissimilarfrom that observed in previous studies documenting fluoride's net effects in clinically inhibiting plaque glycolysis (e.g., Geddes and McNee, 1982; Edgar etal., 1970). In fact, the PGRM results are somewhat more sensitive, owing to the elimination of the complicating tooth mineral component and plaque standardization. What is different in this study is the direct comparison with a proven antimicrobial, chlorhexidine, which itself has shown clinical anticaries action. Since the caries-preventive effect of chlorhexidine must, by definition, be due to antiplaque/antimetabolic effects, the differences in efficacy between the fluoridated toothpaste and chlorhexidine in the PGRM help to dimensionalize the relative anticaries benefits which can be anticipated from fluoride in vivo as an 'antibacterial' agent. At the very least, the PGRM results provide supporting evidence to the idea forwarded by Van Loveren (1990) that fluoride therapies should be performed just prior to cariogenic challenges, in order to maximize the antiplaque component of fluoride's decay-preventive effects. This study, of course, does not provide insight into fluoride's effects on plaque, which might result from multiple exposures of fluoride (Geddes and McNee, 1982), the effects of fluoride in limiting the bacterial activity at lower ph (Eisenberg et al., 1985; Marquis, 1990), ecological shifts in microflora (Marsh and Bradshaw, 1990), or by other antiplaque mechanisms (i.e., such as anti-adhesion). The development of anticaries technologies based upon reducing plaque acidogenicity through specific antibacterial or metabolic inhibitors remains an active

6 VOL. 8(2) MODE OF ANTICARIES ACTION OF FLUORIDE 171 Dentifrice NaF TABLE 2 SURFACE HARDNESS, F UPTAKE, AND MICRORADIOGRAPHY (AZ) CHANGES OBSERVED DURING in situ EXPOSURE AND FOLLOWING SECONDARY ACID EXPOSURE F Uptake 13.1 II AD 3.0J Placebo F Uptake = microdrill-biopsied fluoride measured in jig/cm 2. AD = linearized changes in surface hardness; AD c = following in situ 'remineralization phase'; AD aar = following secondary acid challenge. AZ = Change in AZ from microradiography. Means outside brackets are significantly different at p < AD AZ AZ -606 : TABLE 3 MICRORADIOGRAPHIC CHANGES IN MINERAL OBSERVED in situ FOR ENAMEL AND DENTIN (artificial caries lesions; from Wefel et al., 1989) Dentifrice NaF Placebo All means are significantly different at p < AZ Change-Enamel J AZ Change-Dentin -4166: area in caries research (Van Loveren, 1990). It is likely that combinations of agents, like chlorhexidine and fluoride, may provide advantages in caries prevention due to combined mineral-inhibitory and plaque effects. This will become more relevant in the coming decade, as manufacturers promote the introduction of topical formulations providing gingival health benefits of broad-spectrum antimicrobials combined with fluoride. The role of topical fluoride in affecting bacterial ecosystems, baseline glycolytic activity, and other plaque characteristics needs to be elucidated more fully, and PGRM and other screening techniques may provide a useful means for standardized measurements of these effects. In separate experiments beyond the scope of this paper, the PGRM has been used to differentiate the relative duration and magnitude of antiplaque/antimetabolic effects for a range of agents, including various antimicrobials, surfactants, metal ions, and toothpaste/mouthrinse delivery systems and is being used to assess the general shifts in plaque metabolic activity associated with longer-term topical exposure (White et al, 1993). The Reaction of Topical Fluoride with Enamel and Dentin Importance of Reaction Products to Anticaries Efficacy: Studies Applying the 19-F Solid-state MAS NMR Technique It is accepted that reactions with enamel and dentin minerals contribute in large part to fluoride's anticaries efficacy. Debate continues, however, on the form of fluoride reaction which provides the most efficacy. For a long period, a view was held that fluoroapatite (FAP) formation was the ideal form of reacted fluoride within enamel and dentin. This was based upon the fact that FAP [Ca 10 (PO 4 ) 6 F 2 ] had chemical composition (in the sense of calcium and phosphate composition) equivalent to that of hydroxyapatite (facilitating simple incorporation with saliva ions), with fluoride substitution for hydroxyl providing decreased solubility. This lower solubility was presumed to effect improved acid resistance, resulting in less caries. Today, however, this paradigm is being questioned, as research continues to explore the relative efficacy of solution fluoride vs. mineral bound (lattice) fluoride in preventing demineralization and enhancing remineralization (Arends and Christoffersen, 1990; Featherstone etal, 1990; Margolis and Moreno, 1990; Chow, 1990; White and Nancollas, 1990; ten Cate, 1990) and the anticaries efficacy provided to the teeth through the deposition of minerals other than FAP, such as CaF 2 (White et al, 1988; Rolla and Saxegaard, 1990). These research questions are difficult to study because of the complexity of interaction between solution fluoride and enamel mineral. The mineral phases such as FAP, FHAP [fluorohydroxyapatite: Ca 10 (PO ) 6 OH x F 2. x )] and CaF 2 themselves, for example can contribute as reservoir sources of solution fluoride during periods of cycling de- and remineralization. Furthermore, it is difficult to assess the form of reacted fluoride in dental enamel because of a lack of good analytical/physical techniques applicable to fluoride-apatite analysis. In many instances, this is caused by the fact that fluoride reacts only with a small portion of the crystalline lattice (i.e., the surface atomic layers), thereby providing only limited products for study. In our laboratories, we have applied 19-F Magic Angle Spinning (MAS) NMR to the study of fluoride reaction products with enamel minerals. The 19-F MAS NMR technique has proven to provide unambiguous

7 172 WHFIIETAL ADV DEM RES JULY 1994 measures of fluoride reaction products with apatite, readily distinguishing fluoridated minerals including calcium fluoride andfluoroapatite (Yesinowski andmobley, 1983; Yesinowski et al, 1983; White et al, 1988; Kreinbrink et al, 1990). The NMR evidence that we have gathered suggests that FHAP formation represents the equilibrium mineral phase composition of many fluoridated biological minerals, in agreement with theoretical predictions (Driessens, 1982). However, it is expected that caries protection requires constant re-supply of fluoride reactivity and that caries benefits are at least partially lost without continuous topical application. The development of absolute resistance to caries in the teeth through FAP formation is a myth: Consider that shark enamel, predominantly FAP, is observed to demineralize significantly under in vivo caries conditions without topical fluoride exposure (0gaard et al, 1988). Although the shark enamel demineralization is shown to be less than that of non-fluoridated enamel, in agreement with other comparative studies of FAP and HAP demineralization (Le Geros et al, 1983; Hare et al, 1986; Hoppenbrouwers eta/., 1988), FAP functional resistance to demineralization is only moderately less than that of HAP. Brown et al (1977) have pointed out that the thermodynamic solubility product, K,, of FAP is only slightly less (in thermodynamic termsf than that of HAP (10 61 vs , respectively) and could not in principle account for dramatic increases in 'acid resistance' of enamel. Instead, it is more likely that it is the local concentration of solution fluoride provided by the mineral that provides resistance (Featherstone et al, 1990). This local concentration provided by the mineral can be quite high in carious lesions, since the surfaces of crystals within the enamel can be coated extensively with fluoride following topical treatment and hence behave 'FAPlike'. The most recent data on NSAF suggest that a reaction form of fluoride may exist, independent of other discrete F mineral phases, that can theoretically provide fluoride within the solution phase for both de- and remineralization. It is unknown if this form of fluoride would be superior or inferior to FAP, FHAP, or CaF 2 in shifting local mineral balance toward conditions favoring tooth mineral preservation, and this is an area of current research in our laboratories. Furthermore, it is unknown how quickly NSAF is converted to FHAP (consider the difference in lesion composition compared with that of initially treated enamel) and whether this conversion increases, decreases, or is part of caries protection. It should be noted that NSAF may represent a significant portion of the 'adsorbed' or 'ion-exchanged' fluoride discussed in the earlier literature yet could not be distinguished previously with available chemical or spectroscopic techniques. Thus, for example, in preliminary experiments we have noted that NSAF can be extracted from apatite surfaces by KOH. Based upon the published literature (Caslavska et al, 1975), this chemical result would be interpreted to suggest that the reaction form of the fluoride is calcium fluoride which the NMR shows that it clearly is not. Future research must concentrate on elucidating the effects of NSAF (and the solution chemical manifestations of NSAF formation on the surface) and other fluoride reaction products in our efforts to determine the fluoridation reactions effecting maximum caries protection. 19-F MAS NMR provides a sensitive probe into the mineral components of reacted fluoride which should greatly facilitate these research efforts. Fluoride Anticaries Benefits Remineralization Enhancement or Demineralization Protection?: In situ and ph-c) cling Evidence Supporting Acquired Acid Resistance (AAR) The unique chemistry of fluoride with apatites is responsible in large part for its anticaries effects. In solution, F ions are observed both to increase the rate of calcium phosphate crystallization and decrease the rate of apatite dissolution (White andnancollas, 1990; Featherstone etal, 1990). These effects on the kinetics of apatite reactions are primarily due to effects on the thermodynamics of the calcium phosphate solutions (Brown etal, 1977). Because of this unique chemistry, a very low level of F in solution effects either demineralization protection or remineralization repair of carious enamel, depending upon the coincident ph, calcium, and phosphate activities in the surrounding media. Researchers have long speculated on the relative importance of fluoride's dual (remineralization enhancement/ demineralization inhibition) effects. Today, data from in situ and ph-cycling in vitro models are available which account for the relative proportions of remineralization and demineralization benefits provided by topical fluoride. In recent years, we have accumulated an extensive database on de- and remineralization anticaries effects of fluoride using these protocols. Overall, the data we report here support that the demineralization protection derived from fluoride reactivity in early carious lesions acquired acid resistance (AAR), as popularized by Koulourides (1982) is a primary descriptor of topical fluoride's decay-preventive effects. Enamel or dentin, initially decalcified by plaque acids, becomes more sensitive to reactions with fluoride due to increased porosity and surface area. This increased reactivity permits large amounts of fluoridation to occur, presumably in forms like FAP, FHAP, and NSAF fluoride, highlighted in the preceding section. This fluoridation, In addition to providing repair, conveys a certain degree of acid resistance (in the short term) to the decalcified areas. With continued topical exposure, the areas become arrested and may not cavitate (provided that topical exposure continues). The strong retention of the acquired fluoride is in agreement with the findings of Clarkson et al (1981), who have observed fluoride redistribution within carious enamel exposed to secondary challenges, and who proposed that this phenomenon likely contributed to anticaries activity. The tendency toward arresting lesions rather than providing complete consolidation is supported by additional in vivo and in vitro evidence. In vitro, ten Cate (1992) observed only short periods of remineralization enhancement during the mineralization phase of ph-cycling conditions, whereas demineralization protection extended throughout acid challenges. In vivo, Arends et al (1992) have commented on the slow rates of lesion consolidation and have speculated on the relative benefits of remineralization enhancement and demineralization protection to lesion arrestment. It is important to emphasize that AAR benefits are not to be confused with simple reductions in enamel solubility. The

8 VOL. 8(2) MODE OF ANTICARIES ACTION OF FLUORIDE 173 likely difference between solubility lowering and acid resistance is one of kinetics to provide true acid resistance, the fluoride must be deposited within the carious enamel in a form which is available within the lesion for redistribution through internal equilibration. One current focus of our research is to determine the 'form' of deposited fluoride which provides the greatest AAR benefits following topical treatment. SUMMARY In this paper, we have attempted to show how modern techniques in dental research continue to help us better define mode of action (e.g., the anticaries mechanism) of topical fluoride. Techniques developed for antiplaque testing show that fluoride does not provide a significant 'acute' benefit in reducing plaque acid production, particularly in comparison with a strong (clinically proven) antimicrobial. The use of PGRM in screening plaque samples from subjects in fluoridated areas or using fluoride regimens could provide insights into the more subtle (ecosystem) effects which topical fluoride might elicit on overall plaque acidogenicity. Studies utilizing the 19-F MAS NMR technique show that fluoroapatite FAP is not necessarily the initial reaction product of fluoride formed with dental enamel, and show that a NS AF species may have important contributions to anticaries reactivity of fluoride. We are now extending this technique to the analysis of reaction products of enamel and dentin with various topical systems, including those which are thought to deposit additional fluoride species, like stannous fluorophosphates or calcium fluoride. The net reactivity of these various species can, today, be well-characterized (viz., in a caries-prevention sense) utilizing ph-cycling and in situ models. Studies using these models suggest that topical fluoride prevents caries primarily through the development of increased AAR in initial carious lesions. Recent advances provided by the techniques described here, and others in the literature, place us in a good position to understand more fully the 'mode of action' of fluoride in the future, and to build upon this understanding toward the optimization of anticaries benefits of topical fluoride. REFERENCES Arends JA, Christoffersen J (1990). Nature and role of loosely bound fluoride in dental caries. J Dent Res 69(Spec Iss): Arends J, Nelson DGA, Dijkman AG, Jongebloed WL (1984). Effects of various fluorides on enamel structure and chemistry. In: Guggenheim B, editor. Cariology today. Basel: Karger, Arends J, Dijkman AG, Huizinga E, Van Der Kuyl M, Boerma A, Ruben ],etal.(l 992). The influence of saliva constituents and properties on enamel remineralization in situ. In: Embery G, Rolla G, editors. Clinical and biological aspects of dentifrices. Oxford: Oxford University Press, Bowden GHW (1990). Effects of fluoride on the microbial ecology of dental plaque. J Dent Res 69(Spec Iss): Brown WE, Gregory TM, Chow LC (1977). Effects of fluoride on enamel solubility and cariostasis. Caries Res ll(suppl Caslavska V, Moreno EC, Brudevold F (1975). Determination of the calcium fluoride formed from in vitro exposure of human enamel to fluoride solutions. Arch Oral Biol 20: Chow LC (1990). Tooth-bound fluoride and dental caries. J Dent Res 69(Spec Iss): Clarkson BH, Wefel JS, Silverstone JM (1981). Redistribution of enamel fluoride during white spot lesion formation: An in vitro study in human dental enamel. Caries Res 15: Driessens FCM (1982). Mineral aspects of dentistry. Basel: Karger. Edgar WM, Jenkins GN, Tatevossian A (1970). The inhibitory action of fluoride on plaque bacteria. Further evidence. Br Dent 7128: Eisenberg AD, Wegman MR, Oldershaw MD, Curzon MEJ (1985). Effect of fluoride, lithium or strontium on acid production by pelleted human dental plaque. Caries Res 19: Featherstone JDB, Glena R, Shariati M, Shields CP (1990). Dependence of in vitro demineralization of apatite and remineralization of dental enamel on fluoride concentration. J Dent Res 69(Spec Iss): Geddes DAM, McNee SG (1982). The effect of 0.2 percent (0.48 mm) NaF rinses daily on human plaque acidogenicity in situ (Stephan curve) and fluoride content. Arch Oral Biol 27: Hamilton IR (1990). Biochemical effects of fluoride on oral bacteria. J Dent Res 69(Spec Iss): Hamilton IR, Bowden GH (1988). Effect of fluoride on oral microorganisms. In: Ekstrand J, Fejerskov O, Silverstone LM, editors. Fluoride in dentistry. Copenhagen: Munksgaard, Hare M, Burgess RC, Silva MF (1986). Influence of ambient and enamel fluoride on experimental caries and plaque parameters (abstract). J Dent Res 65:263. Hoppenbrou wers PMM, Groenendijk E, Te warie NR, Driessens FCM (1988). Improvement of the caries resistance of human dental roots by a two-step conversion of the root mineral into fluoridated hydroxy apatite. J Dent Res 67: Koulourides T (1982). Increasing tooth resistance to caries through remineralization. Foods Nutr Dent Health 2: Kreinbrink AT, Sazavsky CD, Pyrz JW, Nelson DGA, Honkonen RS (1990). Fast-magic-angle-spinning 19-F NMR of inorganic fluorides and fluoridated apatitic surfaces. J Mag Res 88: LeGeros RZ, Silverstone LM, Daculsi G, Kerebel LM (1983). In vitro caries-like lesion formation in F containing tooth enamel. J Dent Res 62: Margolis HC, Moreno EC (1990). Physicochemical perspectives on the cariostatic mechanisms of systemic and topical fluorides. J Dent Res 69(Spec Iss): Marquis RE (1990). Diminished acid tolerance of plaque bacteria caused by fluoride. J Dent Res 69(Spec Iss): Marsh PD, Bradshaw DJ (1990). The effect of fluoride on the

9 174 WHITE ETAL. ADV DENT RES JULY 1994 stability of oral bacterial communities in vitro. J Dent Res 69(SpecIss): Moreno EC, Kresak M, Zahradnik RT (1977). Physicochemical aspects of fluoride-apatite systems relevant to the study of dental caries. Caries Res ll(suppl 1): gaard B, Rolla G, Ruben J, Dijkman T, Arends J (1988). Microradiographic study of demineralization of shark enamel in a human caries model. ScandJ Dent Res 96: Rolla G, Melson B (1975). On the mechanism of the plaque inhibition by chlorhexidine. J Dent Res 54(Spec Iss B): Rolla G, Saxegaard E (1990). Critical evaluation of the use of topical fluorides, with emphasis on the role of calcium fluoride in caries inhibition. J Dent Res 69(Spec Iss): ten Cate JM (1990). In vitro studies on the effects of fluoride on de- and remineralization. J Dent Res 69(Spec Iss): ten Cate JM (1992). Mechanistic interactions of dentifrices with de- and remineralization. In: Embery G, Rolla G, editors. Clinical and biological aspects of dentifrices. Oxford: Oxford University Press, Van Loveren C (1990). The antimicrobial action of fluoride and its role in caries prevention. J Dent Res 69(Spec Iss): Wefel J, Jensen ME, Bowman WD, Faller RV, Pyrz JW (1989). In situ evaluation of a polyampholyte dentifrice (abstract). J Dent Res 68:350. White D J (1987). Reactivity of fluoride dentifrices with artificial caries. I. Effects on early lesions: F uptake, surface hardening and remineralization. Caries Res 21: White DJ (1988a). Use of synthetic polymer gels for artificial caries lesion preparation. Caries Res 21: White DJ (1988b). Reactivity of fluoride dentifrices with artificial caries. II. Effects on subsurface lesions: F uptake, F distribution, surface hardening and remineralization. Caries Res 22: White D J (1991). Reactivity of fluoride dentifrices with artificial caries. III. Quantitative aspects of acquired acid resistance (AAR): F uptake, retention, surface hardening and remineralization. J Clin Dent 3:6-14. White DJ, Nancollas GH (1990). Physical and chemical considerations of the role of firmly and loosely bound fluoride in caries prevention. J Dent Res 69(Spec Iss): White DJ, Bowman WD, Faller RV, Mobley MJ, Wolfgang RA, Yesinowski JP (1988). 19-F MAS-NMR and solution chemical characterization of the reactions of fluoride with hydroxyapatite and powdered enamel. Acta Odontol Scand 46: White DJ, Cox ER, Liang N (1993). A rapid screening method (PGRM) for the antiplaque effects of antimicrobials (abstract). J Dent Res 72:271. Wietfeldt JR, Agricola FO, Warner R, Morgan NE, Faller RV (1988). The effect of soluble strontium on the remineralization and fluoride uptake by carious enamel from sodium fluoride (abstract). J Dent Res 67:257. Yesinowski JP, Mobley MJ (1983). 19-F MAS-NMR of fluoridated hydroxyapatite surfaces. J Am Chem Soc 105: Yesinowski JP, Wolfgang RA, Mobley MJ (1983). New NMR methods for the study of hydroxyapatite surfaces. In: Misra DN, editor. Adsorption and surface chemistry of hydroxyapatite surfaces. New York: Plenum Press,

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