ORIGINAL ARTICLE
Gingival temperature measurements with fluoride and nonfluoride elastomeric ligatures K. Aznan, M. Khana and Philip E. Bensonb Sheffield, United Kingdom Introduction: Little is known about the effect of fluoridated elastomerics on gingival health. The aim of this in-vivo study was to compare subgingival temperature measurements near brackets with fluoridated elastomerics with nonfluoridated elastomerics. Methods: This was a prospective, longitudinal, crossover study, involving 12 volunteers. Data, including gingival temperature, gingival crevicular fluid volume, and gingival index scores, were collected weekly from the buccal aspects of 8 teeth for 8 weeks (except for a 1-week washout period). A baseline examination was carried out at week 1. This was repeated at week 2, immediately before placement of orthodontic brackets on all 4 first premolars, which were randomly allocated to receive either fluoridated or nonfluoridated elastomerics. Examinations were repeated at weeks 3 and 4, when the elastomerics were removed. After the washout period, the contrary elastomerics (either fluoridated or nonfluoridated) were placed. Examinations were repeated at weeks 5 and 6 when the elastomerics and brackets were removed. A final examination was performed at week 7. Results: There was a small, but statistically significant, increase in the gingival temperature (P ⫽ .002) after placement of the fluoridated elastomerics. There were no other differences in the markers for gingival health. Conclusions: The mean increase in gingival temperature with fluoridated elastomers was small (0.3°C) and unlikely to be clinically significant, but the implications are discussed. (Am J Orthod Dentofacial Orthop 2007;131:378-83)
T
he placement of an orthodontic bracket can cause worsening of oral hygiene and poor gingival health.1 Histological and anatomical changes occur in gingival microcirculation when gingivitis begins.2 It is assumed that these changes have functional consequences with regard to blood flow that might be significant in the pathogenesis of gingivitis and ultimately periodontitis.3 Because changes in blood flow are associated with local tissue temperature changes, gingival temperature measurement was proposed as a potentially valuable objective method for the diagnosis of periodontal disease.4 Fluoride was shown to reduce the prevalence of caries around orthodontic brackets by encouraging remineralization of enamel.5 It is known to suppress the glycolytic pathway in microbial and animal cells.6 Consequently, fluoride should reduce gingival inflammation. Elastomeric ligatures that claim to release fluoride are commercially available. Several studies suggested that they reduce the prevalence and severity From the School of Clinical Dentistry, University of Sheffield, Sheffield, United Kingdom. a Postgraduate student. b Senior lecturer. Reprint requests to: Philip E. Benson, Department of Oral Health and Development, School of Clinical Dentistry, Sheffield S10 2TA, United Kingdom; e-mail,
[email protected]. Submitted, August 2004; revised and accepted, May 2005. 0889-5406/$32.00 Copyright © 2007 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2005.05.053
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of demineralization, but their effect on gingival conditions was not studied.7,8 If fluoridated elastomerics are shown to lessen gingival inflammation, this will diminish the potential detrimental effects of orthodontic treatment. The aim of this in-vivo study was to compare the subgingival temperature measurements near brackets with fluoridated elastomeric ligatures compared with nonfluoridated elastomeric ligatures. The null hypothesis was that there is no difference in subgingival temperatures between the 2 ligatures. MATERIAL AND METHODS
This was a prospective, longitudinal, crossover study carried out in the orthodontic department at the Charles Clifford Dental Hospital, Sheffield, United Kingdom. Approval was obtained from the local research ethics committee. Sample size was calculated based on data from a previous study.9 This suggested that a sample size of 10 would be sufficient to detect a difference of 1°C with a power of 0.90 and a significance level of 0.05. The final sample included 12 volunteers (6 men, 6 women; mean age, 29.8 ⫾ 7.0 years) with at least 1 premolar in each quadrant, to which an orthodontic bracket could be attached. Subjects who were pregnant or diabetic, were using antimicrobial mouthwashes or any complicating medicine, or had used antibiotics in the last 2 months were excluded. Eight
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teeth were studied in each subject: 4 experimental, premolar teeth with brackets, and 4 control, canine teeth without brackets. The following procedures were carried out (Fig 1). For the baseline examination, the subjects were asked not to eat or drink for 2 hours before the examination. They were seated, and the temperatures of the gingival margins of the premolars and canines in all 4 quadrants were recorded with the PerioTemp RM2 system (Abiodent, Danvers, Mass) (Fig 2) by using the method of Niederman et al.4 First, the subject’s reference temperature was taken by placing the probe lingual to the mandibular second molar, and the subject pursed his or her lips around the handpiece. Then the tip of the temperature probe was placed 1 mm into the mesiobuccal gingival margin of the mandibular left first premolar. The temperature was recorded, and the measurement was repeated on the midbuccal and distobuccal aspects of the same tooth. The highest of the 3 readings was recorded. Temperature measurements were repeated on the canines and the premolars in all 4 quadrants. In addition to the gingival temperature, gingival health was graded according to the modified gingival index described by Lobene et al,10 and the volume of gingival crevicular fluid (GCF) was measured. GCF was collected by using the procedures described by Deinzer et al.11 The gingival sites were isolated with a cheek retractor and cotton wool rolls. A saliva ejector was placed in the subject’s mouth. With an air syringe, a gentle stream of air was directed for 5 seconds along the tooth axis, toward the tooth surface to minimize the effect on the gingival crevice. A gingival fluid collection strip (Periopaper, Interstate Drug Exchange, Amityville, NY) was inserted about 1 mm into the crevice at the midbuccal aspect of the tooth and left in place for 25 seconds. The strip was removed and placed between the electrodes of a Periotron 6000 instrument (Oraflow, Plainview, NY), and the reading was recorded. The reading was converted to a volume measurement by using a standard curve. The standard curve was constructed by pipetting known volumes (0.1-3 L) of serum onto Periopaper and measuring them in the Periotron 6000. The measurements were made in triplicate, and a mean of the 3 readings was used. One week later, the examination was repeated. After this second baseline examination, orthodontic brackets were bonded to premolars in all 4 quadrants of the mouth. Each subject was randomly allocated to receive either fluoridated or nonfluoridated elastomerics on all 4 brackets. The subjects received standard fluoride toothpaste (Boots Dentalcare Specialist, Boots Company PLC, Nottingham, England;
0.22% w/w sodium fluoride, 1000 ppm) and daily fluoride mouthrinse (Fluorigard, Colgate-Palmolive UK Ltd, Manchester, England; 0.05% w/w sodium fluoride 0.025 mg per mL). One week after the placement of the brackets, gingival temperatures and modified gingival index values (but not GCF volume) were recorded. The elastomerics were retained for another week, when a full assessment (including GCF volume) was carried out. The elastomeric ligatures were removed, and each patient had a 1-week washout period. After that, the contrary elastomeric, either fluoridated or nonfluoridated, was placed on the brackets. Gingival temperature and modified gingival index were recorded 1 week after placement of the elastomerics. Two weeks after placement, the elastomerics were removed and stored, and a full assessment was carried out. The brackets and the composite bonding material were removed. A final full examination was carried out 1 week after removal of the brackets. Statistical analysis
The distribution of the data was found to be normal. A mixed-effects analysis of variance (ANOVA) was used to test for differences. The dependent variable was either the gingival temperature measured with the PerioTemp or the GCF volume measured with the Periotron. The random variable was subject. The fixed factors included tooth position (maxillary or mandibular, left or right) and experimental stage (baseline/final and fluoride/nonfluoride elastomeric). The ANOVA was carried out separately for the canines and the premolars. Post-hoc multiple comparisons were done by using the Bonferroni adjustment to correct for type I error. RESULTS
A total of 640 temperature measurements were made (320 on premolars, 320 on canines). The temperatures from 10 subjects were taken each week for 7 weeks, whereas, for 2 subjects, the temperatures at weeks 3 and 5 were not taken. In addition, 480 measurements of GCF volume were collected (240 on premolars, 240 on canines). The results of the ANOVA with gingival temperature as the dependent variable are given in Table I. This shows significance differences for subject, tooth position, and experimental stage for both the premolar (with a bracket) and the canine (without a bracket). Subsequent examination of the data showed that the gingival margin of the maxillary premolars (mean, 34.6°C; SD, 0.9; confidence interval [CI], 34.5°C-34.7°C) was slightly cooler than that of the mandibular premolars (mean, 35.3°C; SD, 0.8; CI, 35.2°C-35.3°C). There
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Baseline examination (gingival temperature, GCF vol, and modified GI) 7 days Second baseline examination, placement of orthodontic brackets and random allocation to either fluoride or nonfluoride ligatures 7 days First examination of first experimental period (gingival temperature, modified GI) 7 days Second examination of first experimental period, elastomerics removed (gingival temperature, GCF vol, and modified GI) 7 days Washout period no elastomeric ligatures Placement of contrary elastomerics (fluoride or nonfluoride) 7 days First examination of 2nd experimental period (gingival temperature and modified GI) 7 days Second examination of second experimental period, elastomerics and brackets removed (gingival temperature, GCF vol, and modified GI) 7 days Final examination (gingival temperature, GCF vol, and modified GI Fig 1. Flow diagram showing sequence of events during experiment.
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Fig 2. PerioTemp RM2 thermometer system.
Fig 3. Chart showing rise in mean temperature during experimental period.
Table I. Results of mixed-effects ANOVA for premolars and canines with gingival temperature as dependent variable showing significance levels for independent variables of subject, tooth position (maxillary or mandibular, left or right), and stage in experiment (baseline, experimental with fluoride elastomeric, experimental with nonfluoride elastomeric, or final)
Table II. Results of mixed-effects ANOVA for premolars and canines with GCF volume as dependent variable showing significance levels for independent variables of subject, tooth position (maxillary or mandibular, left or right), and stage in experiment (baseline, experimental with fluoride elastomeric, experimental with nonfluoride elastomeric, or final)
Subject Tooth position Experimental stage
Premolars
Canines
⬎0.001 ⬎0.001 0.002
⬎0.001 ⬎0.001 0.023
were also slight differences between the left and right sides. The gingival temperature of the right premolars was slightly cooler (mean, 34.8°C; SD, 0.9; CI, 34.7°C34.9°C) compared with that of the left premolars (mean, 35.1°C; SD 0.8; CI, 35.0°C-35.2°C). The post-hoc multiple comparisons showed significant differences in the premolar gingival temperature between the baseline reading and the reading after the removal of the fluoride elastomeric (mean difference, 0.3°C; P ⫽ .010) and between the reading after the removal of the fluoride elastomeric and the nonfluoride elastomeric (mean difference, 0.3°C; P ⫽ .026). In both instances, the gingival temperatures were higher with the fluoride elastomeric. There were no differences between any experimental stages on the canines in the post-hoc comparisons when the Bonferroni adjustment was applied. Figure 3 shows the rise in mean temperature during the experimental period, from a mean baseline reading of 34.8°C (⫾ 0.82) to a peak of 35.2°C (⫾ 0.80) in week 5 and a slight decrease to 35.0°C (⫾ 0.78) at the end. The results of the ANOVA with the GCF volume as the dependent variable are given in Table II. There was a
Subject Tooth position Experimental stage
Premolars
Canines
⬎0.001 0.034 0.124
⬎0.001 0.069 0.784
significant difference in the GCF volume between maxillary and mandibular teeth, but the difference was small (mean difference, 0.02 L). There was no correlation between GCF volume and gingival temperature (Pearson product moment correlation coefficient, – 0.03). Figure 4 shows the median and interquartile ranges for the gingival temperatures of each modified gingival index value; there was no relationship between them. DISCUSSION
In this study, we found increases in the gingival margin temperature near orthodontic brackets with fluoride elastomeric ligatures, compared with brackets with nonfluoride elastomeric ligatures or teeth with no bracket. The mean increase (0.3°C) was small but statistically significant. It is, however, unlikely to be clinically significant. Previous studies with the PerioTemp found a range of differences in the temperatures of healthy and diseased periodontia. Kung et al12 found differences between diseased and healthy sites in the same subjects of 0.47°C in the maxillary canine and 0.67°C in the mandibular canine. Fedi and Killoy13 found differences
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Fig 4. Boxplots showing gingival temperature median and interquartile ranges for each category of modified gingival index recorded.
between diseased and healthy sites in 2 groups of subjects of 1.70°C in the maxillary canine and 1.32°C in the mandibular canine. Niederman et al4 found that the difference in the mean subgingival temperatures between healthy and diseased subjects was 1.35°C. The increase in gingival temperature must be due to the fluoride elastomeric and not the bracket alone, because there was no difference between the baseline readings before placement of the bracket and the readings after bonding a bracket and 2 weeks with a nonfluoride elastomeric ligature. The cause of this increased temperature is unknown. It was noted previously that, when these ligatures are used in the mouth, they swell considerably, probably due to the imbibition of saliva.14,15 This might lead to more plaque bacteria on the ligature that would have an adverse effect on gingival health. However, a recent study found no difference in the percentages of streptococci or anaerobic bacteria between fluoridated and nonfluoridated elastomerics;15 therefore, this must remain speculation. In-vivo studies should make every effort to simulate the real clinical scenario. In this study, the patients were volunteers with only 4 teeth bonded with brackets, and no tooth movement was carried out. Both factors could affect subgingival temperatures; however, we believed that, by reducing the number of potential variables, a clearer idea about the effect of the ligatures was obtained. In addition, because of the commitment in terms of number and frequency of appointments, it would be difficult for real patients to take part. Additional research should be carried out with patients
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undergoing tooth movement with fully bonded appliances to further study how these ligatures perform. Our subjects had healthy gingivae, with no signs of periodontal disease. Most clinical assessments with the modified gingival index showed no or minimal signs of gingival inflammation (99% of assessments were 0 or 1). There was a small mean rise in temperature when a bracket was in situ (0.4°C), although the increase was still present 1 week after debonding. This lack of overt gingival disease is encouraging because it means that deterioration in gingival health is not an inevitable consequence of an orthodontic bracket. GCF volumes remained low throughout the experiment; this indicates good gingival health. This also demonstrates that gingival health can be maintained with an orthodontic bracket in situ. Several studies showed that GCF volume increases during orthodontic treatment and that this is not just related to levels of plaque, gingival inflammation, or pocket probing depth, but to the amount of tooth movement.16,17 The teeth in this study were not being moved; therefore, any GCF increase would be mainly due to increased gingival inflammation. Our subjects were well-motivated adults with only 4 brackets in place; these volunteers do not necessarily represent an adolescent population with fully bonded fixed appliances. Haffajee et al18 found that some temperature differences in the gingivae were related to clinical status, but the correlations were weak. In subjects with poor oral hygiene, the temperature difference between fluoridated and nonfluoridated elastomerics might be greater, and fluoridated elastomerics might be detrimental to gingival health. In these cases, the potential advantages with regard to demineralization might be outweighed by increases in gingival inflammation, but this requires further investigation. CONCLUSIONS
Fluoridated elastomeric ligatures appear to lead to a small, but statistically significant increases in gingival temperature and, by implication, inflammation, compared with nonfluoridated elastomerics. However, this is unlikely to be clinically significant in a well-maintained, healthy mouth. The effects of these elastomerics on gingival health in a group of adolescents should be further investigated.
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3. Holthuis AF, Gelskey SC, Chebib FS. The relationship between gingival tissue temperatures and various indicators of gingival inflammation. J Periodontol 1981;52:187-9. 4. Niederman R, Naleway C, Lu BY, Buyle-Bodin Y, Robinson P. Subgingival temperature as a gingival inflammatory indicator. J Clin Periodontol 1995;22:804-9. 5. Geiger AM, Gorelick L, Gwinnett AJ, Benson BJ. Reducing white spot lesions in orthodontic populations with fluoride rinsing. Am J Orthod Dentofacial Orthop 1992;101:403-7. 6. Hamilton IR. Biochemical effects of fluoride on oral bacteria. J Dent Res 1990;69 (Spec No:660-7);82-3. 7. Banks PA, Chadwick SM, Asher-McDade C, Wright JL. Fluoride-releasing elastomerics—a prospective controlled clinical trial. Eur J Orthod 2000;22:401-7. 8. Mattick CR, Mitchell L, Chadwick SM, Wright J. Fluoridereleasing elastomeric modules reduce decalcification: a randomized controlled trial. J Orthod 2001;28:217-9. 9. Barnett ML, Gilman RM, Charles CH, Bartels LL. Computerbased thermal imaging of human gingiva: preliminary investigation. J Periodontol 1989;60:628-33. 10. Lobene RR, Weatherford T, Ross NM, Lamm RA, Menaker L. A modified gingival index for use in clinical trials. Clin Prev Dent 1986;8:3-6.
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11. Deinzer R, Mossanen BS, Herforth A. Methodological considerations in the assessment of gingival crevicular fluid volume. J Clin Periodontol 2000;27:481-8. 12. Kung RT, Ochs B, Goodson JM. Temperature as a periodontal diagnostic. J Clin Periodontol 1990;17:557-63. 13. Fedi PF Jr, Killoy WJ. Temperature differences at periodontal sites in health and disease. J Periodontol 1992;63:24-7. 14. Wiltshire WA. In vitro and in vivo fluoride release from orthodontic elastomeric ligature ties. Am J Orthod Dentofacial Orthop 1999;115:288-92. 15. Benson PE, Douglas CW, Martin MV. Fluoridated elastomers: effect on the microbiology of plaque. Am J Orthod Dentofacial Orthop 2004;126:325-30. 16. Samuels RH, Pender N, Last KS. The effects of orthodontic tooth movement on the glycosaminoglycan components of gingival crevicular fluid. J Clin Periodontol 1993;20:371-7. 17. Pender N, Samuels RH, Last KS. The monitoring of orthodontic tooth movement over a 2-year period by analysis of gingival crevicular fluid. Eur J Orthod 1994;16:511-20. 18. Haffajee AD, Socransky SS, Goodson JM. Subgingival temperature (I). Relation to baseline clinical parameters. J Clin Periodontol 1992;19:401-8.