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J Dent Res 81(5): 329-333, 2002
© 2002 International and American Associations for Dental Research

RESEARCH REPORT
Biomaterials & Bioengineering

Fluoride Uptake, Retention, and Remineralization Efficacy of a Highly Concentrated Fluoride Solution on Enamel Lesions in situ

W. Buchalla1,2,*, T. Attin3, J. Schulte-Mönting4, and E. Hellwig2

1 Oral Health Research Institute, Indiana University School of Dentistry, Indianapolis, IN, USA;
2 Department of Operative Dentistry and Periodontology, University of Freiburg, Germany;
3 Department of Operative Dentistry and Periodontology, University of Göttingen, Germany; and
4 Institute for Medical Biometry, University of Freiburg, Germany;

*corresponding author, present address, Georg-August-Universität Göttingen, Zentrum Zahn-, Mund- und Kieferheilkunde, Abteilung für Zahnerhaltung, Präventive Zahnheilkunde und Parodontologie, Robert-Koch-Str. 40, 37075 Göttingen, Germany, buchalla{at}med.uni-goettingen.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Repeated topical application of concentrated fluorides is known to reduce caries. Little is known about fluoride retention and remineralization in incipient caries lesions following a single application. We investigated fluoride and the remineralization kinetics of a single application of elmex® fluid (GABA International AG, Münchenstein, Switzerland; 10,000 ppm F) in initial enamel lesions. In this double-blind, placebo-controlled, randomized, crossover in situ study that conformed to good clinical practice, volunteers received intra-oral removable appliances carrying demineralized enamel samples after application of elmex fluid or placebo. After 5 min, 1, 2, 3, and 4 weeks in situ, KOH-soluble fluoride (KOHF), structurally bound fluoride (SBF), mineral gain, and lesion depth reduction were measured. Elmex fluid promoted higher KOHF and SBF at all times, decreased KOHF with time, increased SBF up to 3 weeks, and registered a higher mineral gain than placebo. Volunteers with higher stimulated salivary flow rates had lower fluoride uptake, but higher mineral gain. In conclusion, a single application of highly concentrated fluoride solution increases remineralization.

KEY WORDS: fluoride • carious enamel • remineralization • clinical study • salivary flow rate


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It is accepted that topical fluorides promote remineralization and inhibit demineralization of dental hard tissues (ten Cate, 1990; Ekstrand and Oliveby, 1999). The major reaction product of highly concentrated fluoride preparations is CaF2 (Saxegaard and Rølla, 1988), which is responsible for cariostatic efficacy (Øgaard et al., 1990). However, highly concentrated fluoride products are suspected of clogging the surfaces of incipient caries lesions, thereby impeding remineralization (Øgaard, 1990). In contrast, clinical studies demonstrated that the biannual application of fluoride varnishes and gels results in considerable caries reduction (Helfenstein and Steiner, 1994; van Rijkom et al., 1998). Thus, the aim of the present study was to evaluate fluoride uptake, retention, and the remineralizing efficacy of a single-dose application of a highly concentrated fluoride solution in an in situ study conforming to good clinical practice.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Fig. 1Go provides an overview of the experiment. This placebo-controlled, randomized, double-blind, crossover in situ study was carried out according to the guidelines for good clinical practice (GCP). Volunteers received intra-oral appliances with demineralized enamel specimens twice, for a period of 4 wks each time. Half of the volunteers' specimens received either a single application of elmex fluid or a placebo at the beginning of each period. Specimens were removed weekly for determination of fluoride and mineral content.



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  		Figure 1. Study design. One volunteer's specimen regimen for study period I is shown. Study period II follows the same regimen except that volunteers who received elmex fluid in period I get a placebo and vice versa. Specimens worn by an individual volunteer originated from 5 teeth. Specimens for fluoride and microradiographic analysis removed at the same time in both periods originated from the same tooth (n = 4). Specimens for microradiography had 2 demineralized windows, with one covered with resin to serve as a demineralized control. Specimens for fluoride analysis had the entire surface demineralized.

 
All volunteers were residents of Freiburg, Germany, and surrounding villages with a negligible tap water fluoride content. Before beginning the study, the volunteers gave their written informed consent to the study protocol, which was reviewed and approved by the university's independent ethics committee. Demographic and ethnic data, medical history, and information on previous and concomitant medical and dental treatment were recorded. The oral mucosa and the dentition were clinically investigated. The stimulated salivary flow rate and buffer capacity were measured on three consecutive days by means of a commercially available test (CRT buffer, Vivadent, Schaan, Liechtenstein). Finally, 18 volunteers who fulfilled the inclusion criteria without violating the exclusion criteria (TableGo) were enrolled in the study.


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  		Table. Inclusion and Exclusion Criteriaa
 
Four cylindrical specimens (3 mm diameter) were prepared from each of 90 bovine incisors and gamma-sterilized. The enamel surfaces were ground flat and polished, thereby removing the outer 100 to 200 µm, and flattened from the dentin side to a thickness of 2 mm.

Three narrow strips of adhesive tape (Tesa, Beiersdorf, Hamburg, Germany) were applied parallel to each other on the surfaces of 2 of the 4 enamel specimens originating from 1 individual tooth, leaving 2 equally sized windows. All 360 specimens were immersed in 9 L of unstirred demineralizing solution at 37°C for 6 days. This solution contained 3 mmol/L CaCl2 x 2 H2O, 3 mmol/L KH2PO4, 50 mmol/L C2H5COOH, 6 µmol/L methyldiphosphonate, amounts of KOH to adjust the initial pH to 5.0, and traces of Thymol (Buskes et al., 1985). The adhesive tape was removed from the respective specimens (n = 180), and 1 of the 2 demineralized windows was covered with a dentin-bonding agent (Syntac classic, Vivadent, Schaan, Liechtenstein) for control. The specimens with the control area (n = 180) were intended for mineral gain; specimens without control area (n = 180) were intended for fluoride measurements. Specimens were stored at 100% relative humidity at 8°C in a refrigerator until use.

A removable appliance was fabricated for each volunteer's lower jaw, with a buccal resin wing on each side (Koulourides et al., 1974). Five specimens were mounted in each wing flush with the buccal surface.

The volunteers received the intra-oral appliance (at the beginning of period I) after a one-week wash-out phase. Elmex fluid or a placebo (both GABA International AG, Münchenstein, Switzerland) was applied to the specimens in the appliances of nine volunteers each. Volunteers were assigned to a treatment regimen by means of a computer-generated randomization list. Elmex fluid (pH 3.9) contained 10,000 ppm fluoride from amine-fluoride (9250 ppm fluoride from Olaflur and 750 ppm from Dectaflur), sweetener, flavor, and water. The placebo fluid contained sweetener, flavor, PEG-40 hydrogenated castor oil as emulsifier, potassium parabene and polyaminopropyl biguanide as preservatives, color, and KOH to adjust pH to 6.9. The fluid (0.2 mL) was applied for 20 sec before the appliances were inserted into the mouth. After 5 min in situ, one specimen each for fluoride and mineral content determination was removed, rinsed with distilled water, and stored in 100% humidity. The appliances were kept in situ except during meals and toothbrushing, when kept in 100% humidity.

The recommended toothbrushing procedure included gentle brushing of the intra-oral appliances twice daily without toothpaste to prevent plaque growth. Another set of specimens was removed after 1, 2, 3, and 4 wks in situ. Appliances were refilled with a new set of specimens during a one-week wash-out phase. Period II was carried out in the same way as Period I, but the elmex® fluid-placebo application scheme was performed in reverse.

To determine the KOH-soluble fluoride (Caslavska et al., 1975), we exposed the oral surface of each respective specimen to 1 mL KOH solution (1 mol/L) and agitated it for 24 hrs at 23°C. The solution was neutralized (1 mL 1 mol/L HNO3) and buffered (1 mL TISAB II, Orion Research Corporation, Cambridge, MA, USA). Fluoride content was measured with a fluoride-sensitive electrode (Orion Research Corporation) and calculated in µg/cm2 enamel surface.

The same specimens were used to determine the structurally bound fluoride (Hellwig et al., 1989). A 100-µm layer was ground off, dissolved (0.5 mL 0.5 mol/L HClO3), agitated at 23°C for 1 hr, and buffered with 2.5 mL TISAB II. Fluoride content was measured and calculated in µg/cm3 enamel.

A 90 ± 10-µm-thick slice was prepared perpendicularly to the exposed surface of the specimens dedicated for mineral content analysis. A semi-contact microradiograph of each slice together with an aluminum calibration step wedge was taken. High-speed holographic film (SO 253, Kodak AG, Stuttgart, Germany) was exposed with Cu K{alpha} x-rays at 20 kV and 20 mA for 12 sec. Mineral content {triangleup}Z and lesion depth ld were calculated (Angmar et al., 1963). Sound enamel mineral content was considered 87% by volume. Lesion depth was defined as depth from the specimen surface where 95% of sound mineral content was reached. A Stereo Microscope (Axioplan, Zeiss, Oberkochen, Germany) with CCD-Camera (XC-77CE, Sony, Tokyo, Japan) and a PC with framegrabber and data acquisition and calculation software were used (TMR 1.25e, Inspector Research BV, Amsterdam, The Netherlands). Mineral gain ({triangleup}{triangleup}Z) was calculated as the difference in mineral loss ({triangleup}Z) between the remineralized and the protected demineralized (control) area: {triangleup}{triangleup}Z = {triangleup}Z (control) – {triangleup}Z (remineralized). Lesion depth reduction was calculated accordingly, {triangleup}ld = ld (control) - ld (remineralized).

A repeated-measurement ANOVA model was fitted to the data, and transformations were made where necessary (p <= 0.05). Multiple comparisons were made by sequential analysis; therefore, an {alpha}-adjustment was not necessary. Two hypotheses each were tested for the therapy effect and the time effect of the investigated parameters. For the therapy effect, the hypotheses were: There is no difference between the average values of both therapies (elmex fluid and placebo, H0), and, there is a difference (H1). The hypotheses for the time effect were: There are no differences in changes with time between both therapies (H0), and, there are differences (H1).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
All volunteers were Caucasian but only three were male. At end of the study, all volunteers were between 18 and 50 yrs old (29 ± 7.5, mean ± SD). Their DMFT28 varied between 3 and 21 (10 ± 4.6, mean ± SD). Stimulated salivary flow rate was between 1.1 and 3.7 mL/min (2.1 ± 0.8, mean ± SD), and salivary buffer capacity was high for all volunteers. A few adverse events occurred but were not associated with study medication and had no effect on the study outcomes.

Fluoride Content
The KOH-soluble fluoride (Fig. 2AGo) decreased continuously in the elmex fluid group, from 11.5 to 1.5 µg/cm2 over 4 wks but always remained significantly higher than the placebo control. The fluoride level of the placebo group remained almost stable, around 0.6 µg/cm2. The global therapy effect was significant (p <= 0.001). The time effect (p <= 0.001) showed a significant decrease of KOH-soluble fluoride following treatment.



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  		Figure 2. Means and standard deviations (represented by error bars) from fluoride analyses (A,B) and microradiography (C,D) of the previously demineralized enamel specimens after an in situ period of 5 min, 7, 14, 21, and 28 days following application of elmex fluid or placebo. Asterisks indicate significant (p <= 0.05) differences between elmex fluid and placebo for the given time. (A) KOH-soluble fluoride [µg/cm2] decreased significantly (p <= 0.001) with time for elmex fluid. The SD for elmex fluid after 5 min had to be truncated and is therefore written in brackets. (B) Structurally bound fluoride [µg/cm3] increased significantly (p <= 0.001) up to 3 wks following elmex fluid application, but only minimally in the placebo group. (C) Mineral gain [vol% x µm] increased significantly (p <= 0.01) with time following elmex fluid application. (D) Lesion depth reduction [µm] increased significantly with time (p <= 0.05) in both groups.

 
Elmex fluid application produced a significantly higher amount of structurally bound fluoride at every single time point compared with placebo treatment (Fig. 2BGo). Structurally bound fluoride increased slightly up to 356 µg/cm3 in the placebo group between weeks 1 and 4. Structurally bound fluoride increased over the first 3 wks in the treatment group, but decreased to the one-week level (1695 µg/cm3) after 4 wks. The global therapy effect was statistically significant (p <= 0.001). The time effect was also significant (p <= 0.001), showing that following treatment, structurally bound fluoride was acquired with time.

Correlation of Fluoride Uptake with Salivary Flow Rate
An inverse relation was found between stimulated salivary flow rate and fluoride content of enamel for all times. For example, the correlations of the volunteers' stimulated salivary flow rate with KOH-soluble fluoride after 14 days in situ (Fig. 3AGo) and structurally bound fluoride after 14 days in situ (Fig. 3BGo) are given, indicating a logarithmic relation.



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  		Figure 3. Scatter plot and trend line of the stimulated saliva flow rate (mL/min) vs. (A) KOH-soluble fluoride (µg/cm2) and (B) structurally bound fluoride (µg/cm3) of the fluoridated enamel specimens of all volunteers shown for 14 days in situ (n = 18). Both KOH-soluble (A) and structurally bound fluoride (B) accumulate logarithmically less in volunteers with higher salivary flow rates. A linear relationship can be seen between stimulated salivary flow rate and mineral gain (vol% x µm) shown after 28 days in situ (n = 18) for the elmex fluid group (C) and the placebo group (D).

 
Mineral Gain and Lesion Depth Reduction
Microradiographs showed that no erosion took place and no surface mineral deposits were acquired. All artificially demineralized specimens showed homogenous subsurface lesions. The demineralized control lesions had an average mineral loss of 2072 ± 353 vol% x µm (MW ± SD, n = 180) and an average lesion depth of 77.3 ± 11.6 µm (n = 180). Mineral gain (Fig. 2CGo) increased continuously after fluoride application up to 612 vol% x µm after 4 wks (n = 18). Mineral gain was lower in the placebo group (242 vol% x µm after 4 wks, n = 18). The differences were already significant after 1 wk. Both the global therapy effect and time effect were significant (p <= 0.001). Sixteen specimens in the placebo group demineralized further, but only 2 specimens in the elmex fluid group did. One volunteer in the placebo group produced a high amount of mineral loss after 21 days ({triangleup}{triangleup}Z = -1771 vol% x µm, n = 1), which was out of range. This value was not included for calculation of the placebo's 21-day mean (Fig. 2CGo). Lesion depth reduction (Fig. 2DGo) was higher after the application of elmex fluid, but was not significantly different from that in the placebo group at any given time. As for the mineral-gain results, the mean lesion depth reduction in the placebo group after 3 wks was calculated without one volunteer's outstanding negative value. The global therapy and time effect of lesion depth reduction were weakly significant (p <= 0.05).

Means for the elmex fluid group were larger and standard deviations smaller than for the control (Figs. 2C, 2DGo). The calculated average coefficient of variation (average of [(SD/mean) x 100]) for 1 to 4 wks decreased from 158 (placebo) to 57 (elmex fluid) for mineral gain and from 222 (placebo) to 94 (elmex fluid) for lesion depth reduction. Hence, a single application of elmex fluid on initial enamel lesions not only increased the remineralization but also led to a more stable mineral accumulation with less fluctuation.

Correlation of Mineral Gain with Salivary Flow Rate
A positive relationship was found between stimulated salivary flow rate and mineral gain for both fluoridated and non-fluoridated specimens beginning with 7 days, as can be seen in Figs. 3C and 3DGo.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In situ caries models offer a wide range of possibilities for the study of caries-protective measures (Wefel, 1995; Zero, 1995). The model used in this study was designed to follow both fluoride and mineralization kinetics due to a single application of a highly concentrated fluoride solution in a single experiment. Because of the focus on remineralization, the specimens in situ were not subjected to cariogenic challenges, e.g., plaque growth. The relationship between KOH-soluble and structurally bound fluoride could be studied over time, because all external sources of fluoride were excluded, such as fluoride-rich food or fluoride-containing toothpaste. The order of specimen removal was the same for all volunteers, and there may be concern that specimen position has influenced the outcome. Since the exact influence of the location is unknown, a fixed removal pattern (i.e., mesial specimens removed first, then the most distal specimens, etc.) may not have solved this uncertainty. An individually randomized removal pattern may have been better. We did not choose this method, because of the increased possibility of removal errors.

As in other in vitro and in situ studies, KOH-soluble fluoride in the present investigation was highest following fluoride application, then decreased to a minimum amount after a certain period, thereby serving as a fluoride reservoir (Rølla et al., 1993; Attin et al., 1995). After 4 wks in situ, KOH-soluble fluoride was still significantly higher than in the fluoride-free control group. It can be assumed that KOH-soluble fluoride present after 4 wks still plays an important role, due to its remineralizing capacity (Øgaard et al., 1990).

Structurally bound fluoride increased with time following treatment, which is also in accordance with reports from previous studies (van Rijkom et al., 1998). Although many suggest that firmly incorporated fluoride is not as important as KOH-soluble fluoride with respect to its cariostatic efficacy (Helfenstein and Steiner, 1994), there is evidence that enamel resistance against further demineralization increased with an increase in structurally bound fluoride (Takagi et al., 2000). Interestingly, structurally bound fluoride cannot be increased in intact human enamel simply by increasing the amount of fluoride in a fluoridation product. Calcium phosphates like dicalcium phosphate dihydrate, present in the demineralized enamel of an initial caries lesion, react readily with fluoride to form fluoro-hydroxyapatite (Chow and Brown, 1973), which is less soluble compared with hydroxyapatite. This mechanism may be one reason for the relatively high amount of structurally bound fluoride already present after 5 min. The greater surface area of the lesion due to porosities may be a more important factor for the development of structurally bound fluoride. It is still not fully understood, and the present study does not provide an answer, to what extent these processes contribute to the build-up of structurally bound fluoride and what other processes are involved.

Unexpectedly, a small mineral gain was measurable after only 5 min in situ. Mineral redistribution due to the storage of the specimens in 100% humidity for some days before being sectioned is a possible cause. Mineral gain and reduction of lesion depth increased most during the first 2 wks. It is likely that fluoride made available from the KOH-soluble fluoride reservoir contributed to this remineralization. It is also most likely that fluoride released from the CaF2-like precipitates was incorporated into the gained mineral and accumulated structurally bound. This was not only because the KOH-soluble fluoride fraction decreased with time, but also because no other source of fluoride was involved in the experiment. With KOH-soluble fluoride decreasing and structurally bound fluoride increasing with time, structurally bound fluoride may become the more important cariostatic fluoride fraction by enhancing demineralization resistance and thereby impeding lesion progression rather than promoting remineralization. Although not studied here, this may explain the long-lasting efficacy of highly concentrated fluoride products applied only 2 or 3 times annually. Further studies must evaluate whether a second application, e.g., after 3 months, can reproduce similar mineral gain. It should also be determined whether a lesion will progress under more severe cariogenic conditions. Clinically, there is evidence that, in these circumstances, fluoride application provides only limited caries protection (Ekstrand and Oliveby, 1999).

Both KOH-soluble and structurally bound fluoride was lower in volunteers with higher stimulated salivary flow rates, which may explain interindividual differences in fluoride uptake. This indicates that topically applied fluoride solutions are diluted and washed away by saliva during their tissue-interaction, and that application forms with higher retention rates could be advantageous. Despite a lower fluoride uptake, individuals with higher salivary flow rates gained more mineral. Therefore, salivary flow is the important factor for remineralization, while fluoridation is an effective supportive measure.


   ACKNOWLEDGMENTS
 
We thank GABA International AG, especially Dr. C. Spiegelhalder and Dr. M. Hotze, for supporting the study, Dr. S. Knöfel for her engagement as a second investigator, Dr. N. Umland for specimen preparation, and Mrs. B. Metz for excellent laboratory work. None of the authors is a paid consultant for GABA International.

Received August 22, 2001; Last revision February 11, 2002; Accepted March 18, 2002


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Angmar B, Carlström D, Glas JE (1963). Studies on the ultrastructure of dental enamel. IV. The mineralization of normal tooth enamel. J Ultrastruct Res8:12–23.[Medline]

Attin T, Hartmann O, Hilgers RD, Hellwig E (1995). Fluoride retention of incipient enamel lesions after treatment with a calcium fluoride varnish in vivo. Arch Oral Biol 40:169–174.[Medline]

Buskes JA, Christoffersen J, Arends J (1985). Lesion formation and lesion remineralization in enamel under constant composition conditions. A new technique with applications. Caries Res 19:490–496.[Medline]

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 20:333–339.[Medline]

Chow LC, Brown WE (1973). Reaction of dicalcium phosphate dihydrate with fluoride. J Dent Res 52:1220–1227.[Abstract/Free Full Text]

Ekstrand J, Oliveby A (1999). Fluoride in the oral environment. Acta Odontol Scand 57:330–333.[Medline]

Helfenstein U, Steiner M (1994). Fluoride varnishes (Duraphat): a meta-analysis. Community Dent Oral Epidemiol 22:1–5.

Hellwig E, Klimek J, Albert G (1989). In-vivo Retention angelagerten und festgebundenen Fluorids in demineralisiertem Zahnschmelz. Dtsch Zahnärztl Z 44:173–176.

Koulourides T, Phantumvanit P, Munksgaard EC, Housch T (1974). An intraoral model used for studies of fluoride incorporation in enamel. J Oral Pathol 3:185–196.[Medline]

Øgaard B (1990). Effects of fluoride on caries development and progression in vivo. J Dent Res 69(Spec Iss):813–819.

Øgaard B, Rølla G, Ruben J, Arends J (1990). Relative cariostatic effects of KOH-soluble and KOH-insoluble fluoride in situ. J Dent Res 69:1505–1507.[Abstract/Free Full Text]

Rølla G, Øgaard B, Cruz R (1993). Topical application of fluorides on teeth. New concepts of mechanisms of interaction. J Clin Periodontol 20:105–108.[Medline]

Saxegaard E, Rølla G (1988). Fluoride acquisition on and in human enamel during topical application in vitro. Scand J Dent Res 96:523–535.[Medline]

Takagi S, Liao H, Chow LC (2000). Effect of tooth-bound fluoride on enamel demineralization/remineralization in vitro. Caries Res 34:281–288.[Medline]

ten Cate JM (1990). In vitro studies on the effects of fluoride on de- and remineralization. J Dent Res 69(Spec Iss):614–619.

van Rijkom HM, Truin GJ, van ‘t Hof MA (1998). A meta-analysis of clinical studies on the caries-inhibiting effect of fluoride gel treatment. Caries Res 32:83–92.[Medline]

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Zero DT (1995). In situ caries models. Adv Dent Res 9:214–230.[Abstract]




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