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Influence of diabetes control on gingival health following oral hygiene instructions and use of a triclosan dentifrice.


Purpose: The aim of this cohort study was to evaluate the influence of glycemic control on the gingival bleeding of type 2 diabetic clients after brushing 3 times daily with a triclosan toothpaste for 4 weeks following oral hygiene instructions

(OHI). Methods: Thirty-seven subjects were distributed into 2 groups according to their glycated hemoglobin (HbA1c) levels. The moderately controlled group (MOD) had 18 individuals with HbA1c <9%; the poorly controlled group (PLY) had 19 individuals with HbA1c [greater than or equal to] 9%. After clinical examination, all study participants received OHI which included brushing 3 times daily with a toothpaste containing triclosan using the Bass technique and the daily use of dental floss. Between group differences were analysed using unpaired f tests, while within group differences were calculated with paired t tests. Results: Gingival bleeding index (GBI) was assessed at baseline (MOD = 65.1 [+ or -] 15.1%; PLY = 67.6 [+ or -] 20.2%) and after 4 weeks. At the end of the study period, a significant reduction in GBI was noted in the MOD group (40.2 [+ or -] 18.5%; p < 0.001) but not in the PLY group (56.5 [+ or -] 21.2%). When comparing the 2 study groups, a statistically significant difference (p = 0.017) between groups was found. A significant association was also observed for a 25% GBI reduction in the MOD group in comparison with the PLY group (p = 0.026) as determined with the Fisher's exact test. Conclusions: Type 2 diabetic clients with moderate glycemic control showed improvements in gingival bleeding after oral hygiene instructions and use of a dentifrice containing triclosan. However, no significant improvements were found in the poorly controlled diabetic clients. This regimen seemed insufficient to improve the bleeding status of the poorly controlled group. Incorporating more specific motivational strategies may be needed.


Objectif : Cette etude de cohortes visait a evaluer I'influence du controle de la glycemie sur I'etat gingival des clients diabetiques de type 2 qui, apres avoir recu des instructions d'hygiene buccale (IHB), se sont brosse les dents 3 fois par jour pendant 4 semaines avec un dentifrice contenant du triclosan. Methodes : Trente-sept sujets ont ete separes en 2 groupes en fonction de leur taux d'hemoglobine glycosylee (HbA1c). Le groupe ayant un diabete moderement controle (MOD) comprenait 18 individus au taux de HbA1c < 9 % et le groupe, dont le diabete etait mal controle (MAL), comprenait 19 individus qui avaient un taux de HbA1c [greater than or equal to] 9 %. Apres avoir subi un examen clinique, tous les participants de I'etude ont recu pour instruction de brosser leurs dents 3 fois par jour avec un dentifrice contenant du triclosan en utilisant la technique de brassage Bass et d'utiliser la soie dentaire quotidiennement. Les differences entre les groupes ont ete analysees au moyen de tests t non apparies alors que les differences au sein des groupes ont ete analysees au moyen de tests t apparies. Resultats : L'indice de saignement gingival (ISG) a ete evalue au depart (MOD = 65,1 [+ or -] 15,1%; MAL = 67,6 [+ or -] 20,2%) et apres 4 semaines. Apres 4 semaines de brassage au moyen d'un dentifrice contenant du triclosan, une reduction considerable de I'ISG a ete signalee dans le groupe MOD (40,2 [+ or -] 18,5%, p < 0,001), mais pas dans le groupe MAL (56,5 [+ or -] 21,2%). Lorsque les groupes de I'etude ont ete compares, une difference statistiquement considerable (p = 0,017) a ete trouvee entre les groupes. Une association importante a aussi ete observee chez le groupe MOD en matiere de reduction proportionnelle de I'ISG par rapport au groupe MAL (p = 0,026), telle que determinee au moyen de la methode exacte de Fisher. Conclusions : Les clients diabetiques de type 2 ayant un controle glycemique modere ont presente une amelioration statistiquement considerable en matiere de saignement gingival apres avoir regu des IHB et utilise un dentifrice contenant du triclosan. De telles ameliorations n'etaient pas significatives chez les clients au diabete mal controle. Ce schema therapeutique semblait insuffisant pour ameliorer la sante buccodentaire des individus au diabete mal controle. L'integration de strategies de motivation peut etre necessaire.

Keywords: blood glucose; diabetes; gingivitis; glycated hemoglobin; oral hygiene; triclosan


Type 2 diabetes is a metabolic disease characterized by insulin resistance and inadequate compensatory secretion of insulin. According to the American Diabetes Association, it is the most prevalent form of diabetes, affecting 90% to 95% of diabetic clients. (1) Studies have shown that type (2) diabetes is a significant risk factor for periodontal disease, (2-3) and that periodontitis can also impair the glycemic control of those with diabetes. (4-5) Chronic hyperglycemia observed in clients with poorly controlled diabetes can affect neutrophils, fibroblasts, and collagenases. It can also induce the production of advanced glycation end products (AGEs), which can contribute to greater tissue damage and reduced repair capacity. (6) An improved response to periodontal therapy, along with significant improvements in evaluated clinical parameters, has been demonstrated in well-controlled diabetic clients compared to poorly controlled ones. (7)

Since gingivitis precedes periodontitis, it would be important from a preventive perspective to analyse the effects of gingivitis therapy among individuals with diabetes. There is, however, a lack of studies addressing this issue. (8) Dental treatment including daily plaque removal is of extreme importance in establishing gingival and periodontal health. (9-10) Toothbrushing, associated with the use of dentifrices, is the most common method of oral hygiene used at home by clients and, in most instances, results in removal of dental biofilm, leading to improved gingival and periodontal health." The addition of triclosan, a broad-spectrum antimicrobial agent with low toxicity, to dentifrice formulations is intended to improve plaque control, since it possesses anti-inflammatory effects and has been shown to suppress acute and chronic mediators of inflammation. (12) The most common formulation includes a copolymer (polyvinylmethyl ether maleic acid [PVM-MA]), which enhances the retention of triclosan. (13) Studies have shown significant reduction of gingival indices, including gingival bleeding, in participants with gingivitis using this formulation compared to sodium fluoride dentifrices. (14,15) It is unknown if products containing triclosan would have similar effects on clients with diabetes whose glycemic levels are moderately controlled compared with those who are poorly controlled. Therefore, the aim of this study was to evaluate the influence of glycemic control on gingival bleeding in type 2 diabetic clients following oral hygiene instructions and thrice-daily brushing with a dentifrice containing triclosan over a 4-week period.


Study design

This was a cohort study with a duration of 28 days, in which type 2 diabetic clients attending the City Public Health Department, Sobral, Ceara, Brazil, were distributed into 2 groups according to HbA1c levels. Moderately controlled type 2 diabetic clients (HbA1c <9%) were placed in the group MOD, while the poorly controlled diabetic clients (HbA1c [greater than or equal to] 9%) were placed in the group PLY. (16) This study complies with the recommendations in the STROBE guidelines. (17)


Both males and females diagnosed with type 2 diabetes and presenting with a minimum of 40% gingival bleeding sites were included in the study. Other inclusion criteria were the presence of at least 6 teeth; age 40 years or older; and use of oral hypoglycemic medications. Subjects with periodontitis were also included. The periodontal status of participants was classified according to the Centers for Disease Control and Prevention and the American Academy of Periodontology classification. (18) Smokers, clients who had received periodontal therapy in the past 6 months, those taking medications associated with gingival overgrowth (phenytoin, cyclosporine, and calcium channel blockers), and women who were pregnant or breastfeeding were excluded from this study. All subjects were evaluated at the Public Dental Specialty Center of Sobral, Brazil, between May and December 2012.

The study protocol was reviewed and approved by the Research Ethics Committee of the School of Medicine of the Federal University of Ceara, Brazil. All study participants agreed and signed the informed consent form.


The primary outcome was determined to be the reduction in gingival bleeding 4 weeks after receiving oral hygiene instructions and brushing 3 times daily with a dentifrice containing triclosan, compared with baseline bleeding scores.

Clinical and laboratory procedures

Glycated hemoglobin values were requested at the first visit to determine the glucose control of each study participant. This test was performed at the Public Health Laboratory, Sobral, Ceara, Brazil, using the ion exchange chromatography method (Glico-Teck, Katal Biotecnologica Industria e Comercio Ltda, Belo Horizonte, MG, Brazil). Gingival bleeding was assessed using the gingival bleeding index (GBI) (19) in all teeth, at 2 time points: baseline and 28 days. The GBI evaluates occurrence of bleeding 10 seconds after gentle probing along the gingival crevice at the vestibular, palatine or lingual, mesial, and distal surfaces. The number of positive sites is then expressed as a percentage of the number of gingival margins examined. (19) An experienced periodontist, blind to group distribution, performed all clinical examinations using the UNC 15 periodontal probe (Trinity Industria e Comercio Ltda.-, Sao Paulo, SP, Brazil). If supragingival calculus was present it was removed with an ultrasonic instrument.

After clinical examination, subjects received oral hygiene instructions including on the use of a toothbrush and dental floss. The Bass technique (20) was recommended as the brushing technique, and subjects were instructed to brush for 2 minutes, at least 3 times a day for 4 weeks. A toothbrush (Colgate Professional Extra-Clean, Colgate Palmolive Company, Sao Paulo, SP, Brazil) and toothpaste containing triclosan and the copolymer maleic acid polyvinylmethylether (Colgate Total 12, Colgate Palmolive Company, Sao Paulo, SP, Brazil) were provided. It was estimated that one tube of toothpaste would be sufficient to last the entire study period. No attempt was made to track the frequency of toothbrushing by study subjects.

Study sample size

Sample size was determined (G*Power version 3.0.5, Heinrich-Heine University, Dusseldorf, German) based on a pilot study using the same methodology, which included 24 subjects. Based on the means and standard deviation of test and control groups obtained in the pilot study, the sample size was calculated considering a power of 80% and alpha error of 0.05, which indicated the need for 17 subjects in each group. However, a 20% loss to follow-up was expected, and the sample size was increased to 20 subjects per group who began the study.

Statistical methods

After normal distribution was verified, the unpaired t test was applied to evaluate differences in GBI, HbA1c, age, and tooth count between the 2 groups. The paired t test was applied to evaluate GBI changes after follow-up within the same group. Fisher's exact test was used to compare proportions of gender and periodontal condition between them as well as to evaluate the association between reduction of gingival bleeding and glycemic control. Reduction in gingival bleeding was determined as absolute reduction as well as proportional reduction of 25% and 50% after 4 weeks, and the relative risk was determined for each cut-off. SPSS software (SPSS, IBM Corporation, Armonk, NY, USA) was used for all analysis and significance was set at 0.05.


Thirty-seven subjects completed the study. Of the participants enrolled in the study, 3 were lost to follow-up; 2 in the MOD group and 1 in the PLY group. Baseline data on glycemic control, age, gender, tooth count and periodontal condition are presented according to study groups in Table 1. Statistically significant differences at baseline were observed between groups only for glycemic control (mean HbA1c). Fisher's exact test did not reveal significant differences between groups regarding gender or periodontal condition. In addition, there was an equivalent proportion of different forms of periodontitis in both groups (i.e., mild, moderate, and severe). Baseline values of GBI were not statistically different between the 2 groups (Table 2).

After 4 weeks of brushing with the triclosan dentifrice, a statistically significant reduction in GBI was noted within the MOD group (40.2 [+ or -] 18.5%) (p < 0.001) as illustrated in Table 2 and Figure 1. The same trend was observed in the PLY group (56.5 [+ or -] 21.2%) but was not statistically significant. Between group comparisons at 4 weeks revealed a significant difference, with the MOD group presenting a lower bleeding index than the PLY group (p = 0.017) (Table 2). Figure 2 further illustrates the results with line plots of reductions in bleeding per study participant.

Table 3 presents the number and percentage of participants who had reduced bleeding sites, categorized as absolute, 25% or 50% GBI reduction. Individuals in both groups experienced a reduction in the GBI--89% of subjects in the MOD group and 74% in the PLY group. No association between glycemic control and absolute reduction in GBI between groups was found. However, when the 25% cut-off value for GBI proportional reduction was established, a significant association was observed (MOD = 67%; PLY = 26%), where the relative risk was 2.5 (95% Confidence interval: 1.1-5.7, p = 0.026). Only 3 subjects achieved GBI reductions equal to or greater than 50%, one in the MOD group and 2 in the PLY group with no statistically significant differences observed.


At the commencement of this study, both groups presented with similar gingival bleeding scores despite being in 2 different glycemic control categories. Both the moderately controlled and the poorly controlled groups had elevated GBI levels, with no significant differences between the 2 groups, thus, allowing for a realistic view of the influence of the proposed therapy on the GBI. After oral hygiene instructions and brushing with a dentifrice containing triclosan for 28 days, participants in both groups experienced a reduction in GBI, which reflects improvement in the oral hygiene standards of the study participants. However, a statistically significant reduction in GBI from baseline values was only observed in the moderately controlled group (MOD). When the changes in GBI at 4 weeks were compared between the 2 groups, there was a statistically significant difference demonstrating the PLY group did not respond to the intervention in the same way as did the MOD group. This finding was validated through further analysis of 2 proportional reduction cut-offs points-25% and 50%-revealing that the moderately controlled individuals had 2.5 times better odds of reducing 25% of bleeding sites in comparison with the participants with poorly controlled diabetes. One possible explanation for the lack of a significant reduction in GBI in the poorly controlled group is that the higher HbA1c levels in this group influenced the way they responded to the intervention. If this is the case, these results suggest that more poorly controlled diabetic clients respond differently to oral hygiene practices than those who are moderately controlled.

Since type 2 diabetes and periodontal diseases have been shown to have a bidirectional relationship, (2-5) proper oral hygiene instruction must be recommended to prevent periodontal diseases. Studies have reported that individuals with uncontrolled diabetes tend to present more complications such as periodontitis, which has its onset as gingivitis. (2,3) Literature suggests that, in order to be effective, oral hygiene should include daily mechanical and chemical plaque control by motivated clients. (9,10) Mechanical plaque control is achieved with brushing and flossing, where the dental biofilm is disrupted and physically removed. However, in a systematic review evaluating the effects of plaque control with a manual toothbrush, van der Weijden et al. (11) concluded that the quality of mechanical plaque control was not effective enough to promote resolution of gingivitis. It has been suggested that oral hygiene products containing antimicrobial agents contribute to the resolution of gingivitis, with their effects exceeding those of brushing and flossing. (21) Triclosan is an antimicrobial agent with anti-inflammatory properties that, when associated with copolymer, has its substantivity increased and can reduce gingival inflammation in the proportion of 23% to 49% for a period of 6 months, depending on the gingival index used. (14,15,22)

Study investigators included the use of a dentifrice containing triclosan in this study in order to employ a combination of both mechanical and chemical approaches to plaque control as well as oral hygiene instruction as a motivational strategy. Interestingly, the combination of these 3 strategies was successful with diabetic clients who were moderately controlled, while unsuccessful with those who had poorly controlled diabetes.

To evaluate improvements in oral hygiene, gingival bleeding was chosen as a surrogate clinical parameter in this study and was measured by the GBI. (19) The reason for this choice was the greater clinical significance that this parameter has on periodontal disease. (14,23) Additionally, it is a good indicator of oral hygiene control in the long term, unlike the plaque index which is only indicative of the moment of evaluation. Gingival bleeding has also been considered a significant risk factor for the progression of periodontitis. (23) A longitudinal study, with 26 years of follow up, evaluated gingival bleeding as a risk factor for periodontitis. (23) Lang and colleagues observed that gingival sites that bled had 70% more attachment loss than those that did not bleed. These results allowed the authors to conclude that persistent gingivitis is a risk factor for periodontal attachment loss and tooth loss. (23)

Only one study similar to the current one has been reported. (8) Almas et al. evaluated the effects of oral hygiene instructions on diabetic clients with moderate to severe periodontal disease compared with systemically healthy clients with periodontitis. (8) However, the follow-up period was only 7 days compared with 28 days in this current study. Additionally, the index used to evaluate gingival inflammation (CPITN) differed between these 2 studies. The CPITN used in the Almas et al. study measures not only inflammation but also pocket depth. Improvements in the plaque index were observed in all 3 study groups, but the CPITN score did not change in the diabetic group with advanced periodontal disease. Given the differences in the measuring indices as well as the study length, it is not reasonable to compare the results from this study with the current study results.

In an investigation by Yuen and colleagues (24) exploring the efficacy of plaque removal after oral self-care demonstration among diabetic subjects, the mean percentage of plaque removal was found to be only half of what was expected, and only 10% of participants achieved 50% or more plaque removal. Gingival bleeding, however, was not evaluated and thus also precludes comparision with the current study.

The poorly controlled diabetic group in the current study did not show significant gingival bleeding reduction following oral hygiene instruction and the brushing intervention. This result could be attributed to either biological factors as suggested in the study hypothesis or behavioural factors or the possible interaction between the two. From a biological point of view, chronic hyperglycemia observed in poorly controlled diabetic clients can affect the immune system and induce the production of advanced glycation end products, which can contribute to greater tissue damage and reduced repair capacity. (6) Since those participants with poorly controlled diabetes followed the same study protocol as those in the moderately controlled group, severity of glycemic control can be considered a reasonable explanation for the outcomes of this study.

Insofar as behavioural factors are concerned, clients with uncontrolled diabetes have been reported to be less committed to oral health measures, including oral hygiene and frequency of dental visits. (25) In addition, the manipulation of a manual toothbrush requires hand dexterity, which can be impaired in individuals with diabetes due to hand abnormalities. (24) Tomar et al. reported that the main reason diabetic clients did not visit visiting the dentist was the belief that it was not a necessity. (26) Therefore, educating clients about the effects of diabetes on oral health can be a way of motivating them to improve oral care. (27) Client motivation is an important factor, which may have possibly affected the results of the present study. However, since adherence to the study protocol was not measured, that cannot be assumed. Some authors have reported that many individuals with diabetes do not know that good oral hygiene can be a tool for the control of diabetes. (28,29) Findings from a survey conducted by Moore et al. (28) revealed the majority of respondents, who were adults with diabetes, were unaware of the oral complications associated with the disease. They were also found to be less likely to spend time and money on oral care compared to non-diabetic clients. (28) It is important to note that more women were enrolled in the MOD group in the current study. However, although studies have demonstrated that women seek care more often than men (30) and present better oral hygiene practices, (27,31) in the current study, no significant difference was observed when gender proportion between groups was evaluated.

This study tested the effects of a home care intervention on individuals with both moderately controlled and poorly controlled diabetes. Its findings should be interpreted considering both its limitations and its strengths. This study has 2 major limitations, the first being the decision not to document the adherence of participants to the thrice-daily brushing and dentifrice intervention. The second is the small sample size, which limits its generalizability beyond the current study.

In contrast, the evaluation of gingival inflammation has positive clinical implications since it is more closely related to real life. This study has demonstrated that, for type 2 diabetic clients with moderate glycemic control, frequent oral hygiene home care interventions that include thrice-daily brushing with a dentifrice containing triclosan can improve oral health. This was not the case for those with poor glycemic control. Those individuals with poorly controlled diabetes may need more aggressive interventions including the incorporation of more specific motivational strategies. Further studies are required with larger sample sizes as well as the incorporation of targeted motivational strategies and measurements of adherence in order to determine effective home care control of gingivitis in clients with poorly controlled diabetes.

Since there is a bidirectional relationship between diabetes and periodontal diseases, (2-5) the early identification of diabetes and hyperglycemia can contribute to better outcomes for both diseases. Dental personnel must be aware of this condition and help to identify undiagnosed or poorly controlled diabetes. To facilitate such a diagnosis, a new screening tool has been developed for the chairside testing of gingival crevicular blood collected at the dental visit that can be used to screen for diabetes and monitor glycemic control. (32) Additionally, if clients who present with diabetes risk factors receive a more detailed explanation of their condition and specific follow-up, improved client outcomes may be achieved. (33)


Within the limitations of this study, it can be concluded that daily use of a dentifrice containing triclosan following oral hygiene instruction in type 2 diabetic clients with moderate glycemic control produced a significant reduction in gingival bleeding over a 4-week period. However, the sample size of 37 study participants limits the generalizability of the findings. Gingival bleeding in clients with poorly controlled diabetes did not show improvements by the end of the observation period. This finding suggests that oral health professionals, mainly dental hygienists, may need to incorporate more specific motivational strategies into their preventive regimens to improve the home oral care efforts of this vulnerable population.


This study was sponsored by grants from the Brazilian Research Agencies CAPES (PROCAD NF 2313/2008) and FUNCAP (266010009).


* Type 2 diabetes is a risk factor for periodontal disease, and periodontitis can impair glycemic control

* Maintaining good oral hygiene instruction in clients with diabetes is essential to the control and prevention of periodontal disease

* Oral hygiene instruction coupled with specific motivational strategies may be particularly beneficial to individuals with poorly controlled diabetes


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Katia Linhares Lima Costa *, DDS, MS, PhD; Zuila Albuquerque Taboza *, DDS, MS; Riehelle Soares Rodrigues *, DDS, MS; Gisele Barreto Angelino ([section]), DDS; Virginia Regia Souza da Silveira ([dagger]), DDS, MS, PhD; Rodrigo Otavio Rego **, DDS, MS, PhD

* Department of Clinical Dentistry, Graduate Program in Dentistry, Federal University of Ceara, Fortaleza, Brazil

([section]) School of Dentistry, Federal University of Ceara, Sobral, Brazil

([dagger]) Assistant professor, Department of Dentistry, School of Dentistry, Federal University of Ceara, Sobral, Brazil

** Associate professor, Department of Dentistry, School of Dentistry, Federal University of Ceara, Sobral, Brazil

Correspondence: Dr. Rodrigo Otavio Rego;

Submitted 14 February 2017; revised 5 October 2017; accepted 10 October 2017

Caption: Figure 2. Plots of GBI changes between baseline and 4 weeks in MOD and PLY groups
Table 1. Baseline demographic and clinical characteristics

                                                       PLY group
                                MOD group            [greater than
                               (HbA1c <9%)         or equal to] 9%)

Number of participants             18                     19

HbA1c (%)                   7.6 [+ or -] 0.8     10.7 [+ or -] 1.6 (a)
  (Mean [+ or -] SD)
Gender                     5 males, 13 females    10 males, 9 females
Age (Mean [+ or -] SD)      58.1 [+ or -] 7.6      56.8 [+ or -] 8.5
Tooth count                 14.6 [+ or -] 7.1      14.2 [+ or -] 6.4
  (Mean [+ or -] SD)
Gingivitis                       7 (39%)                8 (32%)

Periodontitis                   11 (61%)               11 (58%)
Mild                             4(22%)                 4(21%)
Moderate                         5(28%)                 4(21%)
Severe                           2(11%)                 3(16%)

HbA1c = glycated hemoglobin; SD = standard deviation

(a) statistically significant (p < 0.001, ttest)

Table 2. Changes in GBI from baseline to 4 weeks

                               MOD group
                                (n = 18)

Baseline GBI (%, SD)    65.1 ([+ or -] 15.1)
Four-week GBI (%, SD)   40.2 ([+ or -] 18.5) (a)

                               PLY group
                                (n = 19)

Baseline GBI (%, SD)    67.6 ([+ or -] 20.2)
Four-week GBI (%, SD)   56.5 ([+ or -] 21.2) (b)

(a) Significant difference between baseline and 4-week data
(p < 0.001 by paired t test)

(b) Significant difference between MOD and PLY groups
(p = 0.017 by unpaired t test)

Table 3. Reduction of bleeding sites (number and proportion
of subjects) per group and statistical analysis

                                 MOD group   PLY group   Fisher's exact
Reduction in GBI                 (n = 18)    (n = 19)    test (p value)

Absolute                         16 (89%)    14 (74%)      0.404
[greater than or equal to] 25%   12 (67%)     5 (26%)      0.026 (a)
[greater than or equal to] 50%    1 (6%)      2 (11%)      0.588

                                 Relative risk
Reduction in GBI                   (95% CI)

Absolute                         1.9 (0.6-6.3)
[greater than or equal to] 25%   2.5 (1.1-5.7)
[greater than or equal to] 50%   0.5 (0.1-5.3)

GBI = Gingival Bleeding Index; CI = confidence interval

(a) Statistically significant

Figure 1. Mean values of Gingival Bleeding Index (%)

       Baseline   Final

MOD    65.1       40.2
PLY    67.6       56.2

(a) Significant within group difference between baseline
and 4-week data (p < 0.001 by paired t test)

(b) Significant difference between MOD and PLY groups
(p = 0.017 by unpaired t test)

Note: Table made from bar graph.
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Author:Costa, Katia Linhares Lima; Taboza, Zuila Albuquerque; Rodrigues, Riehelle Soares; Angelino, Gisele
Publication:Canadian Journal of Dental Hygiene
Geographic Code:3BRAZ
Date:Oct 1, 2017
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