Biomimetic and protective effects of bioactive toothpastes on eroded enamel surfacesAbstract
This study aimed to evaluate the effectiveness of bioactive toothpastes in remineralizing eroded enamel surfaces in vitro. Bovine enamel blocks (n = 48) were obtained and classified into untreated, demineralized, and treated areas. Specimens were randomly classified into six groups (n = 8 each): fluoride-free toothpaste (NCT), Colgate Total 12 (PCT), Sensodyne Repair and Protect (SRP), Sensodyne Pronamel (SPE), Regenerador + Sensitive (RGS), and RGS/calcium booster (RCB). The specimens were subjected to erosive pH cycling for 5 days for 4 times/day (90 s) and treated with toothpaste slurries (1:3) for 1 min. The Vickers hardness (50 g/10 s) and percentage surface hardness recovery (%SMHR) were calculated. Furthermore, the topography and roughness (Ra) of the enamel surface were evaluated using a 3D non-contact optical profilometer, along with the tooth surface loss (TSL). Data were statistically analyzed using analysis of variance or Tukey’s test (significance: 5%). The %SMHR of the SRP and NCT groups were significantly lower than those of the other groups (p < 0.05). Ra was higher when the eroded area was treated with SRP and SPE (p < 0.05). Treatment with RGS, PCT, and SPE favored the recovery of the enamel surface compared with the NCT group (p < 0.05). The best TSL results were obtained with treatment with RGS, followed by PCT and SPE (p < 0.05). The RCB group showed statistically equivalent results for surface hardness recovery and TSL (p > 0.05). Conclusively, PCT and RGS toothpastes were more effective in remineralizing the enamel surface.
Dental Enamel; Hardness; Surface Properties; Tooth Remineralization; Toothpastes
Introduction
The development of advanced toothpastes with an optimal percentage of fluoride to prevent caries, along with an understanding of consumer preferences, offers consumers an advantage over earlier fluoride technologies.1 In addition to the availability of toothpastes with specific indications in the market, multipurpose toothpastes with various therapeutic effects have also been introduced.2 Consequently, with technological advancements, the purpose of brushing teeth has evolved beyond just refreshing one’s breath.
Currently, toothpaste systems can be categorized as one-step, multi-functional, or two-step systems based on their clinical applications. Two-step toothpaste systems include a conventional toothpaste combined with other bioactive ingredients in a second tube.3 Brushing with these two components can simultaneously or sequentially remove oral biofilms and prevent other oral diseases, including tooth sensitivity, periodontal disease, tooth loss, and oral mucosal lesions.4 Furthermore, a subsequent application of other commercial products, such as whitening toothpastes, is recommended to achieve a whitening effect to remove stains and bleach darkened teeth, followed by a cleaning effect with fluoride toothpaste.5
Conversely, multi-functional all-in-one toothpaste systems contain bioactive ingredients in a single formula and provide multiple effects, including tooth cleaning, preventing gingivitis, treating oral mucosal lesions, and remineralizing dental tissues.6,7 Notably, one-step systems called desensitizing toothpastes can be applied to exposed dentin.8 However, despite a variety of specific reasons for selecting a toothpaste, consumers are attracted to all-in-one products that minimize dental sensitivity while promoting enamel remineralization.2
The goal of developing new products and advancing technology is to reduce the negative effects of conventional fluoride treatments by enhancing remineralization and reducing the enamel demineralization abilities of formulations.9 However, compared with alternative remineralization techniques, fluoride action is still regarded as the gold standard,10 and despite the development of technology for enamel recovery using tissue engineering, the ability to replace and mimic enamel tissue remains limited.11 Considering the unique structure of tooth enamel and the dynamic process by which ions are lost and restored in the hydroxyapatite lattice,12 des-remineralization process can be enhanced by substituting small levels of ionic species at different sites of the hydroxyapatite molecule.13 Consequently, biomimetic agents, known as fluoride boosters, are added to toothpaste formulations.14 These agents effectively remineralize the enamel by acting as calcium and fluoride carriers inside dental tissues and reinforce the tooth structure by increasing the size of hydroxyapatite crystals, making it less soluble and porous.9 Therefore, these agents are termed F-boosters, as they contain bioactive compounds based on hydroxyapatite and calcium phosphate, which increase fluoride effectiveness and accelerate remineralization, the process of absorbing calcium and phosphate into the demineralized tooth structure that leads to mineral gain.15 Treating the eroded dental tissues with these bioactive-containing products may form or repair a less organized, poorly mineralized layer on the enamel and dentin.16
One strategy relies on incorporating silicon into the remineralizing enamel structure to increase hydroxyapatite bioactivity.17 Notably, silicon-based toothpastes facilitate the formation of an enamel-like inorganic-oriented structure on the surface of natural enamel, 16 which serves as a calcium and phosphate ion precipitation site, generating calcium silicate, triggering the development of hydroxyapatite and other minerals, and accelerating remineralization.18 Few studies have evaluated the effectiveness of calcium boosters on the remineralization of eroded enamel surfaces. A previous in vitro study evaluating the regenerative and protective effects of fluoride–silicon-rich toothpastes associated with a calcium booster demonstrated that this combination regenerated the dental tissues, remineralized the enamel structure, and occluded the dentin tubules.19 The present study aimed to evaluate the biomimetic and protective effects of bioactive toothpastes on the remineralization of eroded enamel surfaces in vitro. We assumed the null hypothesis that the tested bioactive toothpastes would have no significant biomimetic or protective effect on the remineralization of eroded enamel surfaces.
Methods
Toothpaste selection
We selected commercially available products containing fluoride and other bioactive ingredients (Sensodyne Repair and Protect [SRP], Sensodyne Pronamel [SPE], Regenerador + Sensitive [RGS], and RGS/calcium booster [RCB]) as indicated by the manufacturers. A fluoride-free product was used as the negative control toothpaste (NCT), whereas Colgate Total 12 (PCT) was used as a positive control. The pH of the toothpaste slurries (1:3, w/v in distilled water) prepared in four different samples was determined immediately using a pH electrode (AK95, Akso, São Leopoldo, Brazil) calibrated with standards (pH 4.0, 7.0). The characteristics of the products are listed in Table 1.
Specimen Preparation for the Hardness Analysis
Forty-eight enamel blocks (4.0 × 4.0 × 6.0 mm) were obtained from bovine incisors using a water-cooled rotating diamond wheel (Isomet, Buehler Ltd., Evanston, USA). The sample size was calculated using Sealed Envelope Ltd., considering a significance level (alpha) of 5% and a power (1-beta) of 80%; a sample size of at least 48 enamel blocks was included in the present study. The enamel blocks were embedded in epoxy resin (EpoxiCure Epoxy Resin and Hardener, Buehler, Lake Bluff, USA). The surfaces were then wet-polished with 600 and 1200-grit SiC paper at low and high speeds, respectively, using a polishing machine (Single Grinder Polisher, Buehler, Lake Bluff, IL, USA). The final polishing was performed with 1-μm diamond paste and wet felt wheels (Buehler, Lake Bluff, USA). The baseline surface microhardness (SH0) was measured using a microhardness tester (HMV, Shimadzu, Kyoto, Japan) with a Vickers indenter under a static load of 50 g for 10 s to select enamel blocks with a 392 ± 30 Vickers hardness number (VHN).
Erosive lesion formation
The enamel blocks were subjected to erosive demineralization as previously described.20 One-third of the block surface was covered with two layers of nail varnish (Risque, Niasi, Taboão da Serra, Brazil), referring to the untreated area. After 5 min of sonication in water using an ultrasonic device, the enamel blocks were individually immersed in 0.1% citric acid (pH 2.5) for 30 min at room temperature under gentle horizontal agitation (60 rpm). The acidic solution was replaced every 5 min (30 mL/specimen). Thereafter, the blocks were subjected to surface microhardness (SH1) using the same parameters as described previously.21
For the remineralization pH cycling model, the second to third surface area of the enamel blocks was covered with two layers of nail varnish (Risque, Niasi, Taboão da Serra, Brazil), referring to the erosion lesion area. The enamel blocks were subjected to erosive remineralization as previously described. The specimens were immersed in 0.1% citric acid (pH 2.5) for 90 s four times a day, for five consecutive days. After each demineralization cycle, the specimens were rinsed with deionized water for 10 s and stored in artificial saliva22,23 (pH 6.8, 30 mL/specimen, at 25 °C) for 2 h. After the first and last erosive challenges of the day, the specimens were treated with their respective slurries (toothpaste:deionized water, 1:3 w/w; 2 mL/enamel specimen) for 1 min under agitation. In the RCB group, the blocks were exposed to equal portions of both fluoride and booster toothpaste for 1 min, following the manufacturer’s instructions. At the end of each erosion cycle, the specimens were stored overnight in artificial saliva. Citric acid was replenished after each erosive challenge, and saliva was replenished daily.
Enamel hardness analysis
After pH cycling, enamel surface hardness (SH2) was determined using the same parameters as above. The hardness of the three areas of each specimen was tested, with a distance of 100 μm between each indentation performed in the center of the thirds. Five indentations were made in each area (n = 5). The percentage of surface hardness recovery (%SMHR) was calculated using the following formula (equation 1):24
Enamel surface roughness and topography
The enamel surface of the specimens, according to the experimental groups, was scanned with an optical profilometer (Taylor Hobson - CCI MP, West Chicago, Illinois, USA). The analyses were performed using a 0.25 mm cut-off with a 20× magnification lens at a constant speed of 1 mm/s in the XYZ mode (1024 × 1024 pixel resolution). A Gaussian filter (FALG) was used according to ISO 16610-61. The length of each scan covered the central slab area of 0.86 (X-axis) × 0.86 mm (Y-axis). Three measurements per specimen were obtained and averaged to determine the Ra value (in μm). We also examined the topography of the enamel surface. The tissue surface loss (TSL) was calculated for each specimen, first after acid treatment (untreated/eroded - TSL1) and then after toothpaste treatment (untreated/treated - TSL2), using the following formula (equation 2):
All measurements were performed in triplicate, and the mean values were used to represent the final surface profile.
Statistical analysis
Data were statistically analyzed using the SPSS package for Windows (version 21.0; SPSS, Inc., Chicago, IL, USA). Shapiro–Wilk and Levene’s tests were used to determine the normality and homogeneity of variance, respectively. No data transformation was performed, as the data demonstrated equal variances and a Gaussian distribution. The following tests were performed: 1) analysis of variance (ANOVA) followed by Tukey’s test for analyzing differences in SH0, SH1, SH2, and %SMHR between the groups; 2) repeated measures ANOVA followed by Bonferroni’s test for analyzing the surface roughness variables; and 3) ANOVA followed by Tukey’s test for determining the difference between TSL after erosion and after treatment. The significance level for all the analyses was set at 5%.
Results
The average means and standard deviations for the surface microhardness variables SH0, SH1, SH2, and %SMHR are presented in Table 2. On the mineralized surface, the SH0 means (baseline enamel surface microhardness) varied from 389.7 for SRP to 393.6 VHN for NCT, with no significant differences between the groups (p > 0.05). Furthermore, SH1 means (post-demineralization surface hardness) varied from 286.0 for RCB to 306.8 VHN for RDC, with no significant differences between the groups (p > 0.05). For SH2 (surface hardness after pH cycling/treatment), the highest and lowest means were 328.9 for RGS and 270.6 for SRP, respectively. Except for the NOVAMIN-containing toothpaste (SRP group), a significantly higher mean SH2 was observed when the enamel was treated with the fluoride toothpaste than with the control fluoride-free toothpaste (p < 0.05). For %SMHR, all fluoride toothpastes exhibited significantly higher means than the NCT group (p < 0.05) except for the SRP.
The enamel surface roughness results after toothpaste treatment are presented in Table 3. The lowest and highest enamel surface roughness (Ra2) was observed after brushing for the NCT (0.265) and SPE (0.596) groups, respectively. During pH cycling, treatment with SRP and SPE significantly affected enamel roughness, with the highest Ra means (p > 0.05).
Figure 1 presents the means of the difference between the roughness of the eroded and treated areas following treatment with different toothpastes. An increase in surface roughness was observed for all toothpastes after treating the eroded surface, except for the RCB group, which showed a reduction in surface roughness.
Means and standard deviations (vertical bars) of the difference in roughness of the eroded area in the treated area for the tested toothpastes.
Figure 2 illustrates the enamel surface topography according to area (untreated, sound enamel; eroded demineralized area; and treated area) using representative 3D topographical images representing the results of each group.
Figure 3 displays the tooth surface loss (TSL), calculated as the difference between the eroded area (TSL1) and the area treated with different toothpastes (TSL2). Notably, the eroded enamel surfaces were recovered by treatment with the bioactive toothpastes, with the best results obtained using treatment with RGS, followed by PCT and SPE (p < 0.05). Notably, the RGS and RCB groups exhibited intermediate means, statistically equivalent to the NCT and the groups that best recovered the eroded enamel (RGS, PCT, and SPE). The SRP and NCT groups exhibited significantly lower means for enamel recovery (p > 0.05).
Means of the unetreated to eroded areas (TSL1) and unetreated to treated (TSL2) areas and the means of tooth surface loss (TSL), calculated based on the difference between TSL1 and TSL2 for different toothpastes.
Discussion
This in vitro study evaluated the biomimetic and protective effects of bioactive toothpastes on the remineralization of eroded enamel surfaces. Despite the expected effectiveness of fluoride toothpastes in preventing erosion and managing tooth structure loss, recent investigations have raised concerns regarding the rising incidence of erosive wear.25 The preventive potential of fluoride toothpastes in erosive and abrasive models has been graded as moderate and low for conventional and stannous fluoride toothpastes, respectively.26 However, a previous review concluded that the protective and remineralizing effects of fluoride have been clearly demonstrated in various studies and that calcium and phosphate ions derived from saliva are indispensable for fluoride action. Furthermore, the protective action of fluoride was attributed to its accelerating effect on remineralization but not to its incorporation into the tooth.27 Consequently, boosters are added to toothpastes containing hydroxyapatite- and calcium phosphate-based bioactive compounds28 to increase fluoride effectiveness and accelerate remineralization.15
Our results demonstrated that most of the tested toothpastes helped recover enamel hardness after the erosive challenge (Table 2). Notably, treatment with bioactive compounds-containing toothpastes significantly affected the surface microhardness recovery %SMHR, except for SRP. The %SMHR after treatment with RGS, SPE, and RCB significantly reversed the erosion compared with the treatment with the negative control (NCT group). The highest %SMHR of 33.5% was obtained using treatment with the fluoride-silicon-rich toothpaste RGS (Table 2).
The superior outcomes for RGS can be explained by the biomimetic effects of its constituents on the surface morphology of the treated specimens. This toothpaste uses proprietary REFIX technology, a multi-functional phosphate-based dental gel in an acidified stabilized phosphate/fluoride complex established in the presence of saliva.21 A previous investigation29 reported that the use of toothpaste with a REFIX base facilitates the development of a silicon-enriched mineral layer on the enamel surface owing to the formation of calcium, phosphorus, and sodium complexes. Notably, the mechanical characteristics of silicon-enriched hydroxyapatite are affected by the substitution of phosphate groups with silicon,30 and substituting silicon into remineralizing hydroxyapatite increases the bioactivity and apatite-forming ability of hydroxyapatite when combined with fluorine and phosphate groups.17, 31 Previous in vitro studies16, 32 have also demonstrated the formation of a calcium- and silicon-rich mineral layer in specimens treated with the same toothpaste, supporting our findings. These results are also corroborated by clinical studies.33,34
In our study, the %SMHR for treating the specimens with a combination of RGS and a calcium booster (RCB) was 22.2%, with no significant difference compared with RGS alone. The fact that the acidity of the REFIX-containing toothpaste changed when the specimens were treated with equal portions of both products may explain this difference in %SMHR (33.5% for RGS and 22.2% for RCB). The pH of the slurry of the RGS and RCB was 4.73 and 7.94, respectively, whereas the RCB mixture had an intermediate pH of 6.6. Although this may affect the %SMHR, a previous in vitro study19 reported that a calcium booster associated with a fluoride silicon-rich toothpaste (same as the RCB group) could prevent the mineral loss of dental tissues, and a significant mineral change was observed in both the enamel and dentin after treatment for 5 days. Furthermore, RCB could facilitate the formation of a protective silicon-enriched mineral layer on both the enamel and dentin surfaces, corroborating the findings of the present study. Even at a less acidic pH, extra calcium provided by calcium boosters would saturate calcium in both the acquired pellicle and saliva relative to the tooth. Therefore, increasing calcium saturation may enhance the presence of fluoride on the tooth surface and promote fluoride-induced remineralization.35
Equivalent means of %SMHR were observed for the SPE (22.8%) and the positive control groups (PCT: 25.5%) (p < 0.05). The manufacturer claims that SPE strengthens and protects enamel, rehardens acid-weakened tooth enamel, and aids in the overall remineralization of teeth owing to its optimized fluoride formulation associated with other bioactive compounds. However, in a previous study,36 SPE presented unfavorable results compared with other commercial products indicated to prevent the clinical effects of dental erosion. Notably, the authors highlighted that the interaction between NaF and KNO3 may reduce the bioavailability of fluoride, affecting enamel recovery after an erosive challenge. Similar unfavorable results were observed in another study37 wherein no protective deposits against erosion were observed on the enamel surface following treatment with SPE.
In the present study, the positive effect observed for SPE was not observed for SRP manufactured by the same manufacturer as that of SPE. Notably, %SMHR for the fluoride toothpaste SRP was -29.0%, indicating a significantly lower enamel surface hardness following treatment with this product (270.6) than after the erosive challenge (296.5), which was approximately similar to that observed following treatment with the fluoride-free toothpaste (-20.5%). SRP is claimed to control dentin hypersensitivity and features a technology based on sodium and calcium phosphosilicate (patented as NovaMin), an amorphous inorganic compound classified as particulate bioactive glass with medium-sized particles of < 20 μm.38 According to the manufacturer’s information, these characteristics favor a series of chemical reactions that occur when the product is in an aqueous solution. Subsequently, interactions with this solution facilitate the formation of a carbonated hydroxyapatite layer (that is, an insoluble mineralized layer) on the dentin surface. A previous in vitro morphologic study39 reported incomplete protection of the enamel surface even after the formation of a hydroxyapatite-like layer, with visible remaining eroded areas, following SRP treatment.
In this study, the surface roughness of the treated enamel varied depending on the toothpaste used. Most toothpastes presented a pH that was nearly neutral to alkaline, with an acidic pH for RGS. Notably, extreme pH values, such as those observed for RGS (4.7), may negatively affect the surface roughness. Except for the RCB group, which favored a reduction in surface roughness (from 0.338 to 0.285), all toothpastes exhibited an increase in surface roughness. In general, the synergism of the chemical and physical characteristics, such as pH, particle size, and distribution, of toothpastes may affect the enamel surface roughness after treatment during pH cycling. The increase in enamel surface roughness after treatment was significantly higher in the SRP and SPE groups (p < 0.05), which presented alkaline (8.8) and neutral (7.2) pH, respectively.
Interestingly, TSL results indicated a recovery of the enamel surface topography after treatment, irrespective of the bioactive toothpaste used. A significantly higher TSL on treating the eroded area was observed for RGS, followed by PCT and SPE (p < 0.05). RCB exhibited intermediate means for TSL that were statistically equivalent with the NCT, RGS, PCT, and SPE groups (Figure 3). The SPE and NCT groups exhibited significantly lower mean values for enamel recovery (p > 0.05).
Bioactive toothpastes have been developed to accelerate the remineralization process or minimize the demineralization of dental tissues, particularly in the event of repetitive erosive challenges. However, our results underscore the limitations of this in vitro methodology. Moreover, abrasives may also affect the tooth structure, although the specimens were not brushed in the present study. Some of the bioactive abrasives, such as silica, calcium carbonate (CaCO3), and calcium phosphate dihydrate (CaH2 PO4.2H2O), interact with the tooth structure after ionization in saliva. In addition, as previously explained, even in the absence of active toothbrushing, the following factors can still alter the surface roughness of enamel surfaces after treatment with toothpaste: pH (highly acidic or alkaline toothpastes can affect the enamel mineral content), chemical composition (certain active ingredients or additives in toothpastes can interact with the enamel and influence its surface characteristics), presence of abrasives (some highly abrasive particles in toothpaste might settle on the enamel surface), fluoride concentration (higher fluoride concentrations can lead to the formation of a calcium fluoride-like layer on the enamel), and bioactive ingredients (remineralizing agents can deposit on the enamel surface). Despite these limitations, efforts have been made to simulate the variables in the oral environment, especially pH cycling, which influences the demineralization and remineralization processes in both in situ and in vivo analyses.40 In vitro analyses allow better regulation of conditions at reduced costs for assessing the effectiveness of new products designed to remineralize enamel tissue. In addition, several analyses, including surface hardness, percentage of surface hardness recovery, topography and roughness of the enamel surface, and TSL, can be performed on the same specimens. These methods have been validated to assess the in vitro remineralization of dental enamel.
In the present study, the fluoride-silicon-rich REFIX technology presented the most promising results compared with treatments using other commercial products. These results can be explained based on a previous study,27 which concluded that fluoride treatment under acidic conditions leads to partial dissolution (demineralization) of the enamel surface (hydroxyapatite), followed by the reprecipitation of fluoride-containing minerals. Notably, the thickness of this fluoride-containing layer increases with increasing fluoride concentration, favored by a low pH value.27 In addition to forming a superficial mineralized layer on the enamel, RGS exhibited a significantly higher surface microhardness recovery with fewer effects on surface enamel roughness and higher means of tooth surface gain, demonstrating its ability to better resist acid dissolution following the erosive challenge.
Conclusions
All bioactive fluoride-containing toothpastes, except for the SRP, evaluated in this study could recover the enamel surface hardness following the erosive challenge compared with the PCT groups. The REFIX-technology toothpaste (RGS), regardless of an associated calcium booster (RCB), induced the least changes in surface enamel roughness on treating the eroded enamel. Furthermore, the biomimetic and protective effects of bioactive toothpastes on eroded enamel surfaces allowed for tooth surface gain following treatment. This gain in enamel surface topography was particularly high for the RGS, SPE, and PCT groups. Our findings indicated variable effects of tested products on eroded enamel surfaces. Further in situ and in vivo studies are warranted to investigate the biomimetic and protective effects of these bioactive products on dental substrates.
Acknowledgments
This study was supported by the Federal University of Paraiba for supporting the research (Internal Call for Research Productivity, Propesq/PRPG/UFPB No. 03/2020, Project No. PVG 13306-2020). The authors thank the Federal University of Paraiba for technical support.
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Publication Dates
-
Publication in this collection
20 Dec 2024 -
Date of issue
2024
History
-
Received
5 Mar 2024 -
Accepted
20 June 2024 -
Reviewed
14 Aug 2024
Ra0: initial roughness; Ra1: roughness after erosive challenge; Ra2: roughness after treatment; NCT: fluoride-free toothpaste (negative control); PCT: Colgate Total 12 (positive control); SRP: Sensodyne Repair and Protect; SPE: Sensodyne Pronamel; RGS: Regenerador + Sensitive; RCB, RGS associated with a calcium booster.