1Faculty of Dentistry, University of Hong Kong, 3/F, Prince Philip Dental Hospital, 34 Hospital Road, Hong Kong SAR; and 2School of Stomatology, Sun Yat-sen University, Guangzhou, China; *corresponding author, edward-lo@ hku.hk

J Dent Res 91(8):753-758, 2012

AbstrAct To investigate the effectiveness of topical fluorides in preventing fissure caries, we conducted a ran- domized controlled trial with parallel groups. In total, 501 children (1,539 molars, 3,078 sites), mean age 9.1 years, who had at least one sound permanent first molar with deep fissures or fis- sures with signs of early caries were recruited. They were randomly allocated among four groups: (1) resin sealant, single placement; (2) 5% NaF varnish, semi-annual application; (3) 38% silver diamine fluoride (SDF) solution, annual applica- tion; and (4) placebo control. Follow-up examina- tions were conducted every 6 months by a masked examiner. After 24 months, 485 children (97%) were examined. Proportions of pit/fissure sites with dentin caries in the sealant, NaF, SDF, and control groups were 1.6%, 2.4%, 2.2%, and 4.6%, respectively. A multi-level logistic regression anal- ysis accounting for the effects of data clustering and confounding factors showed that fissures in any of the three treatment groups had significantly lower risks of carious cavity development into dentin than did controls (p < 0.05). We concluded that placement of resin sealant, semi-annual appli- cation of NaF varnish, and annual application of SDF solution are all effective in preventing pit and fissure caries in permanent molars (ClinicalTrials .gov number CT01446107).

KEY WOrDs: dental caries, pit and fissure, preventive dentistry, fluoride, resin sealant, children.

IntrODuctIOn

Dental caries is common among schoolchildren worldwide (Petersen, 2003) and occurs mostly in molars in the permanent dentition (Batchelor and Sheiham, 2004; Sheiham and Sabbah, 2010). This poses a significant problem in populous developing countries, such as China (Lo et al., 1999; Hu et al., 2011). There is a great need to implement effective programs to prevent caries in the pits and fissures of the permanent molars of schoolchildren. In rural or less-developed areas, where resources and dental care services are limited, innovative and cost-effective preventive methods are called for.

Systematic review has shown that dental sealant is effective for the pre- vention of fissure caries (Ahovuo-Saloranta et al., 2008). However, the good performance of sealants depends on high-quality placement aided by electri- cally powered devices (Beauchamp et al., 2008). Therefore, using this method in areas where access to dental clinics is limited may be problematic.

Sodium fluoride (NaF) varnish has been shown to be effective in prevent- ing dental caries in children and adolescents (Marinho et al., 2002; Marinho, 2009). However, few clinical studies have been conducted specifically to assess its effectiveness in preventing caries in the pits and fissures of perma- nent molars (Hiiri et al., 2010).

A recent systematic review found silver diamine fluoride (SDF) solution to be effective in preventing and arresting dental caries in young children (Rosenblatt et al., 2009). So far, only one study reported on its use to prevent caries in permanent first molars (Llodra et al., 2005).

The aim of this study was to investigate the effectiveness of resin fissure sealant, NaF varnish, and SDF solution in preventing pit and fissure caries in permanent molars of schoolchildren. The null hypothesis was that all three treatments had no caries-preventive effect compared with a placebo control.

MAtErIAls & MEthODs

A randomized clinical trial with parallel groups was implemented in April 2008 in a suburb of Guangzhou in southern China. There was no systemic fluoridation, but approximately 90% of the toothpastes on sale contained fluoride. Ethical approval was granted by the University of Hong Kong (www.ClinicalTrials.gov #NCT01446107).

Children studying in grades 2 or 3 in the four largest primary schools of the study site were invited. Children with parental consent were clinically examined by one trained dentist in the schools. Generally healthy children who had at least one sound permanent first molar with deep fissures or fissures with signs of early (enamel) caries viewed as wet, with opacities and discoloration, similar to ICDAS code 2 (Ismail et al., 2007), were included. Molars with caries in dentin and fissures with potential dentin caries indicated by DIAGNOdent (KaVo, Biberach, Germany) readings ≥ 40 (Lussi et al., 2004) were excluded.

randomized trial on Fluorides and sealants for Fissure caries Prevention

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754 Liu et al. J Dent Res 91(8) 2012

Each included molar was assessed at 2 sites (upper molar — mesial pit/fossa and distal-palatal groove; lower molar — occlusal fissure and buccal pit/groove). The recorded status included fissure morphology (deep/shallow), sign of early caries (yes/ no), and DIAGNOdent reading. Information on the child’s toothbrushing habits, snacking habits, and dental visit history was collected through a questionnaire.

An assistant, using computer-generated random numbers, allocated the children individually among four groups: (1) seal- ant — placement of resin sealant (Clinpro Sealant, 3M ESPE, St. Paul, MN, USA) with no replacement; (2) NaF — semi-annual application of a 5% NaF varnish (Duraphat, Colgate-Palmolive Ltd, Waltrop, Germany); (3) SDF — annual application of a 38% SDF solution (Saforide, Toyo Seiyaku Kasei Co. Ltd., Osaka, Japan); or (4) placebo control — annual application of water. Treatments were applied by another dentist according to group allocation.

In the sealant group, the tooth was isolated with cotton rolls. Pits and fissures were etched with 37% phosphoric acid for 15 sec, washed with water, and then dried with gently blown air. The sealant was applied and then light-cured. Complete setting and retention of sealant were confirmed before the child left. In the NaF varnish and the SDF solution groups, the tooth was isolated with cotton rolls. The topical fluoride agent was painted on the pits/fissures by means of a small disposable brush. The child was instructed not to drink or eat for half an hour.

Status of the molars, including sealant retention and develop- ment of caries into dentin (ICDAS codes 4-6) (Ismail et al., 2007), was assessed every 6 mos by the same blinded examiner using disposable mouth-mirrors attached to an intra-oral LED

light and CPI probes. Sites with sealant fully retained were regarded as sound. The primary study outcome was carious cav- ity development into dentin. A 10% random sample was re- examined during every examination to monitor intra-examiner reproducibility. Carious cavities in the study molars were treated with placement of ART restorations.

In sample size calculation, an 80% survival (no dentin caries) of the molars receiving fissure sealant was anticipated, and a 10% absolute difference in caries incidence among groups was regarded as clinically significant. Based on a 5% statistical sig- nificance level and an 80% power, calculated by K*C cross- tabulation in SamplePower 2.0, 950 teeth were required. This number was multiplied by [1 + (m-1)ICC] to adjust for the clustering effect of several teeth within one child (Murray et al., 2004). The intraclass correlation (ICC) was estimated to be 0.2, and 3 molars were expected in each child (i.e., m = 3). With an anticipated 10% drop-out rate, the numbers of teeth and children required at baseline were 1,478 and 493, respectively.

Data Analysis

A chi-square test was used to compare the caries incidence of the four groups with the statistical software SPSS 19.0 (SPSS Inc., Chicago, IL, USA). To study the effects of various factors and to account for clustering of data, we performed a multi-level logistic regression analysis using generalized estimating equa- tion (GEE) modeling with SAS 9.2 software (SAS Institute Inc., Cary, NC, USA). Outcome was recorded at the tooth-site level, and a two-level structure (level 1 — pit/fissure; level 2 — child) was adopted. The dependent variable was the presence of dentin

Figure. Flow of participants until 24 mos in this study (n = number of participants, N = number of teeth; 2N = number of fissure sites).

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J Dent Res 91(8) 2012 Topical Fluorides and Sealant in Caries Prevention 755

caries at the 24-month examination. Independent variables included those at the participant and tooth levels—treatment (sealant, NaF, SDF), gender (boy/girl), grade (2/3), snacking (frequent or not), toothbrushing (frequent or not), baseline den- tal visit history (yes/no), baseline dmft score, and molar location (upper/lower)—as well as variables at the site level—early car- ies at baseline (present/absent), DIAGNOdent reading (high/ low), and fissure morphology (shallow/deep). Interaction effects between and among the independent variables were considered. Exchangeable and independent correlation structure of the clus- tering of sites in each child was also assessed, and the model yielding the highest QIC value was selected as the final model.

rEsults

Among the 1,000 invited children, 499 were excluded because they did not fulfill the inclusion criteria (Fig.). In total, 3,078 pit/ fissure sites (1,539 molars) in 501 children (50% boys), mean age 9.1 yrs, were included. In total, 485 children with 1,491 molars and 2,982 sites (97%) were followed for 24 mos. Eighteen sites in three children were excluded because orth- odontic bands had been attached to the involved teeth. The only

complaint received was a transient bitter taste associated with SDF, and no adverse side-effects were observed.

Regarding distribution of participant- and site-level factors in the four groups at baseline (Table 1), proportionately more children in the sealant group than in other groups had visited a dentist or consumed snacks once a day or less (p < 0.05). There were no significant differences in other factors.

Intra-examiner reliability was excellent (kappa > 0.9). At the 24-month examination, 46% of the sealants were partially or fully retained. Proportions of pit/fissure sites with dentin caries were not significantly different (p > 0.05) in the sealant, NaF, and SDF groups, at 1.6%, 2.4%, and 2.2%, respectively (Table 2). The percentage of sites with dentin caries in the control group, 4.6%, was significantly higher than those in the 3 treatment groups (p = 0.002). The site-level prevented fractions (PF) were 65%, 48%, and 52% for sealant, NaF varnish, and SDF solution, respectively.

The GEE logistic regression analysis results showed that sealant placement (OR = 0.32, p = 0.017), NaF varnish (OR = 0.43, p = 0.033), and SDF solution (OR = 0.44, p = 0.029) were protective factors, while lower molar (OR = 2.43, p = 0.009), early caries at baseline (OR = 3.09, p < 0.001), high baseline

table 1. Distribution of the Study Children and Tooth Sites in the Four Groups According to Different Factors at Baseline

Group

Factors Sealant NaF SDF Control p-value

Participant-level Gender 0.150

- boy 56 (45%) 54 (44%) 69 (55%) 69 (54%) - girl 68 (55%) 70 (56%) 56 (45%) 59 (46%)

Grade 0.686 - grade 2 63 (51%) 57 (46%) 54 (43%) 60 (47%) - grade 3 61 (49%) 67 (54%) 71 (57%) 68 (53%)

Dental visit history 0.024 - yes 60 (48%) 74 (60%) 80 (64%) 84(66%) - no 64 (52%) 50 (40%) 45 (36%) 44 (34%)

Snacking habit 0.005 - once a day or less 108 (87%) 86 (69%) 95 (76%) 91 (71%) - twice or more a day 16 (13%) 38 (31%) 30 (24%) 37 (29%)

Toothbrushing habit 0.560 - once a day or less 54 (44%) 64 (52%) 55(44%) 60 (47%) - twice or more a day 70 (56%) 60 (48%) 70 (56%) 68 (53%)

site-level Fissure morphology 0.175

- shallow 110 (15%) 124(16%) 133 (17%) 104 (13%) - deep 632 (85%) 646 (84%) 647 (83%) 682 (87%)

Early caries 0.939 - yes 257 (35%) 267 (35%) 280 (36%) 272 (35%) - no 485 (65%) 503 (65%) 500 (64%) 514 (65%)

DIAGNOdent reading 0.508 - 16 to 39 291 (39%) 299 (39%) 281 (36%) 308 (39%) - 15 or lower 451 (61%) 471 (61%) 499 (64%) 478 (61%)

Site location 0.224 - upper molar 338 (46%) 348 (45%) 372 (48%) 392 (50%) - lower molar 404 (54%) 422 (55%) 408 (52%) 394 (50%)

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756 Liu et al. J Dent Res 91(8) 2012

DIAGNOdent reading (OR = 4.85, p < 0.001), and baseline dental visit experience (OR = 2.19, p = 0.016) were risk factors for the development of dentin caries (Table 3).

DIscussIOn

In this study, effectiveness of the treatments was studied at the pit/fissure level. The 24-month incidence rates of dentin caries in the three treatment groups were lower than that in the control group. Thus, the null hypothesis was rejected. This is supported by the multi-level logistic regression analysis when the effects of data clustering and selected confounding factors were accounted for.

In this study, the prevented fraction (PF) of NaF varnish application after 24 mos at the tooth level was 39%. This is similar to the 38% PF found in a comparable study (Bravo et al., 1996). Hardman et al. (2007) did not find significant caries reduction when NaF varnish was applied to molars in school- children, and they suggested the poor response and low caries incidence rates of the study sample as possible explanations. It has been suggested that children should be restricted from drink- ing and eating for half an hour (Adair, 2006) or 4 hrs (Hawkins et al., 2003) after fluoride varnish application. In this study, due

to practical reasons (children would return home for a meal after school), the children were asked not to eat for at least half an hour. It is not clear to what extent this affected treatment effectiveness.

The tooth-level PF of the SDF solution application in this study, 41%, is lower than the PF of 65% found in a study con- ducted in Cuba (Llodra et al., 2005). This may be due to the difference in application frequency, once vs. twice per yr, between this and that study.

In this study, the tooth-level PF of resin sealant 24 mos after placement was 60%, which is lower than those reported in most of the previous studies (approximately 80%) (Ahovuo-Saloranta et al., 2008). This may be related to the lower sealant retention rate in this study compared with other studies, 46% vs. 80% (Muller-Bolla et al., 2006; Ahovuo-Saloranta et al., 2008). Most likely, the field setting and the use of portable dental equipment in this study were less than optimal for good placement of resin seal- ant. Difficulty in moisture control during sealant placement was sometimes encountered, which may have affected the retention of the resin-based fissure sealants, a main factor for its effectiveness. Under more optimal working conditions, a higher sealant reten- tion rate and a higher PF would be expected (Gooch et al., 2009).

The incidence of fissure caries in the control group in this study is in line with the recently reported national average

table 3. Final Model of the Multi-level GEE Logistic Regression (nsubject = 482, Nfissure = 2,964)

95% C.I. for Exp (B)

Factors B SE Chi-square p-value Exp (B)* Lower Upper

DIAGNOdent reading 16-39 1.58 0.33 22.87 < 0.001 4.85 2.54 9.27 With early caries at baseline 1.13 0.30 13.96 < 0.001 3.09 1.71 5.58 Lower molar 0.89 0.34 6.83 0.001 2.43 1.25 4.72 Dental visit history at baseline 0.78 0.33 5.76 0.016 2.19 1.15 4.15 Study group 8.23 0.042

- SDF vs. Control -0.82 0.39 4.56 0.029 0.44 0.21 0.93 - NaF vs. Control -0.84 0.39 4.76 0.033 0.43 0.21 0.92 - Sealant vs. Control -1.12 0.47 5.72 0.017 0.32 0.13 0.82

Intercept -5.66 0.45 < 0.001

*Exp(B) = Odds ratio (OR).

table 2. New Dentin Caries in the Four Study Groups at the Participant, Tooth, and Site Levels and Prevented Fractions at the 24-month Follow-up

Sealant NaF SDF Control

No. with new caries Participant 9 15 15 21 Tooth 11 16 17 28 Fissure site 12 17 17 35 Caries incidence (%) - Participant* 7.4 12.8 12.2 16.9 - Tooth# 3.0a 4.4a 4.4a 7.4b

- Fissure site# 1.6c 2.4c 2.2c 4.6d

Prevented fraction (%) Tooth 60 41 41 --- Fissure site 65 48 52 ---

Chi-square test, *p > 0.05, #a < b, p = 0.04; #c < d, p = 0.002.

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J Dent Res 91(8) 2012 Topical Fluorides and Sealant in Caries Prevention 757

prevalence of dental caries in 12-year-old children in China (Hu et al., 2011), but it is low compared with the results of previous studies conducted among high-caries-risk populations (Songpaisan et al., 1995; Bravo et al., 1996). This low 24-month caries incidence may be partially explained by today’s slower dental caries progression rate (Whelton, 2004). Similarly, low levels of fissure caries incidence have also been observed in schoolchildren at similar ages in other countries (Rugarabamu et al., 2002; Parner et al., 2007). In addition, the oral health education delivered to all of the children and the popularity of fluoridated toothpaste in the area of this study may have had an effect on decreasing caries development in the study population. This may in turn have led to a reduced difference in caries development among the four study groups.

Multilevel modeling with a Bayesian approach for survival analysis has been used to analyze hierarchical clustered interval- censored data from longitudinal clinical studies (Harkanen et al., 2002; Wong et al., 2005). In survival analysis, event development is linked with time. For events that take a long time to develop, such as carious cavity development in dentin, substantial bias may arise in survival analysis if the observation period is relatively short and the event occurrence rates are low for the early portions of the time scale. Since the caries progression rate in this study was low, the advantage of survival analysis may not be achieved. Therefore, multilevel logistic regression modeling, a method that uses single-time-point outcome data, was adopted.

In this study, although some of the background factors were not balanced at baseline, the possible interactions among these factors, together with the factor of treatment, were considered in the multivariate GEE logistic modeling. After the GEE model was used to adjust for the effects of data clustering and con- founding factors, the factor of treatment remained in the final model. The effectiveness of the 3 study treatments in preventing pit and fissure caries in permanent molars was confirmed.

In the final model, it was found that study teeth with early car- ies at baseline, as indicated by clinical signs or a DIAGNOdent reading ≥ 16, were more likely to develop dentin caries after 24 mos. The lower molars in this study were also at a higher risk than the upper molars. This is in agreement with other epidemiological findings (Batchelor and Sheiham, 2004). These molars are at a higher risk of developing caries and warrant a higher priority for prevention (Beauchamp et al., 2008). In this study, children who had a dental visit history at baseline developed more dental caries during the 24-month period than those who did not. These chil- dren probably had a higher previous caries experience, which is commonly considered as a risk indicator for new caries develop- ment (Bader et al., 2008; Sarmadi et al., 2009).

The 2-year results of this clinical trial provide some support for the use of topical fluoride applications for the prevention of caries in the permanent molars of schoolchildren, given that it is their major dental disease. In areas or populations where resources and availability of dental care service do not present a major problem, resin sealant placement may be the preventive treatment of choice among schoolchildren. However, in less-developed areas, where economic consideration and resource limitations are more influen- tial in decision-making, this may not be possible. Application of NaF varnish or SDF solution to the pits and fissures of the molars may be considered as an alternative preventive method to

the placement of a fissure sealant. Topical fluoride application is technically simple, does not require powered dental equipment, and may be performed by trained auxiliary health personnel. These are advantages for its use in dental public health programs or commu- nity projects for the prevention of dental caries in schoolchildren, especially those living in places where there are shortages of dental personnel and necessary equipment for the placement of fissure sealant. Before recommendations can be made regarding these new alternative methods for fissure caries prevention, however, more information is needed from studies on longer-term outcomes and economic evaluation, such as their cost-effectiveness.

Based on the 24-month results and within the limitations of this study, it is concluded that the 3 preventive methods—placement of resin sealant, semi-annual application of NaF varnish, and annual application of SDF solution—are effective in preventing pit and fissure caries in permanent molars. Furthermore, they are not sig- nificantly different from one another in their effectiveness.

AcKnOWlEDgMEnts

This article is based on a thesis submitted to the Faculty of Dentistry, University of Hong Kong, in partial fulfillment of the requirements for the PhD degree. This study was supported by the Hong Kong Research Grants Council (#HKU/771207M). The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

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