Q U I N T E S S E N C E I N T E R N AT I O N A L
PERIODONTOLOGY
Tobias T. Hägi
The effects of erythritol air-polishing powder on microbiologic and clinical outcomes during supportive periodontal therapy: Six-month results of a randomized controlled clinical trial Tobias T. Hägi, Dr Med Dent1/Petra Hofmänner, Dr Med Dent, MAS2/Sigrun Eick, PD Dr Med Dent2/ Marcel Donnet, PhD 3/Giovanni E. Salvi, Prof Dr Med Dent 4/Anton Sculean, Prof Dr Med Dent, MS, Dr hc5/Christoph A. Ramseier, Dr Med Dent, MAS6 Objectives: To characterize the physical characteristics of a new low abrasive erythritol powder (EPAP) and to evaluate its influence on the clinical and microbiologic parameters over a period of 6 months in patients undergoing supportive periodontal therapy (SPT). Method and Materials: Prior to the clinical application, the particle size and abrasion level of EPAP were compared to glycine air-polishing powder (GPAP) ex vivo. Subsequently, 40 chronic periodontitis patients previously enrolled in SPT were randomly assigned into two groups for the treatment with subgingival EPAP or repeated scaling and root planing (SRP). At baseline (BL), bleeding on probing positive (BOP+) sites with probing pocket depth (PPD) of ≥ 4 mm but no detectable calculus were defined as study sites. During SPT, these sites were either treated by EPAP or SRP at BL, 3, and 6 months (3M, 6M). When indicated, additional SRP was provided. Plaque Index, BOP, PPD, clinical attachment level (CAL), and
subgingival plaque were evaluated at BL and 6M. Results: EPAP yielded lower abrasiveness and smaller particle sizes when compared to GPAP. In 38 patients completing the study, EPAP and SRP resulted in significant reductions of BOP% (EPAP, 40.45%; SRP, 42.53%), PPD (EPAP, -0.67; SRP, -0.68), and increase of CAL (EPAP, 0.48; SRP, 0.61) while at 6M no statistically significant between-group differences were observed (P > .05). Microbiologic evaluation revealed minor shifts in the composition of the subgingival biofilm without influence on periodontopathogenic bacteria. Conclusion: The subgingival use of EPAP by means of an air-polishing device may be considered safe and may lead to comparable clinical and microbiologic outcomes to those obtained with SRP. Clinical Relevance: The subgingival use of EPAP appears to represent a promising modality for the removal of subgingival biofilm during SPT. (Quintessence Int 2015;46:31–41; doi: 10.3290/j.qi.a32817)
Key words: air polishing, bleeding on probing, erythritol, hard tissue loss, supportive periodontal therapy
1
Postgraduate Student, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
5
Professor and Chairman, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
2
Associate Professor and Head of Oral Microbiology Laboratory, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
6
Assistant Professor, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
3
Researcher, EMS Electro Medical System, Nyon, Switzerland.
4
Associate Professor, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
VOLUME 46 • NUMBER 1 • JANUARY 2015
Correspondence: Prof Anton Sculean, Freiburgstrasse 7, 3012 Bern, Switzerland. Email: [email protected]
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The majority of longitudinal clinical studies in periodontal research confirm the significance of supportive periodontal therapy (SPT) for the maintenance of periodontal health.1-5 Well-established treatment protocols for SPT include:6-9 • repeated scaling and root planing (SRP) in periodontal sites with remaining signs of periodontitis (ie, bleeding on probing positive [BOP+] and periodontal pocket depth [PPD] ≥ 4 mm) • debridement of all areas with detectable soft and hard deposits • motivation of the patient to improve their daily selfperformed plaque control. SRP is traditionally performed using metal curettes or sonic/ultrasonic devices, both presenting a comparable outcome.10,11 However, SRP by hand instrumentation or ultrasonic devices need to be performed carefully as their frequent use may lead to dental hard tissue loss.12-18 The introduction of an air-polishing device using glycine air-polishing powder (GPAP) for the removal of supraand subgingival biofilm has been shown to result in less dental hard tissue loss and greater reductions of colony forming units in pockets with 3 to 5 mm PPD compared to the treatment with hand instruments.19 Moreover, no significant differences were found between SRP or ultrasonic instrumentation and GPAP in periodontal pockets on a short-20 and mid-term basis.21,22 The abrasiveness of glycine powder was further demonstrated to be approximately 80% lower than the bicarbonate air-polishing powder previously used.23-26 The latest development of a specially designed nozzle for subgingival air-polishing devices led to a reduction of the working pressure along with an air jet directed perpendicularly to the root surface.20-22 Since none of the published studies reported any adverse events related to the use of subgingival airpolishing devices, it was suggested that for the removal of supra- and subgingival dental biofilms this treatment regime may be superior to hand instrumentation, particularly with respect to patient comfort, dental hard tissue loss, and time efficiency. Recently, a new low abrasive erythritol powder (EPAP) with comparable physical properties to GPAP
32
was introduced for subgingival air polishing. Erythritol, a non-toxic, chemically neutral, and completely watersoluble polyol is widely used as an artificial sweetener and as a food additive.27 Due to its comparable particle size to that of glycine and its promising chemical characteristics allowing the binding of antiseptic substances, it was recently suggested to be suitable for subgingival biofilm removal.28 Additionally, recently published data demonstrated an inhibitory effect of erythritol to some periodontopathogenic bacteria such as Porphyromonas gingivalis.29 Very recent data indicate that subgingival air polishing with EPAP resulted in short-term clinical outcomes comparable to SRP. Moreover, the use of EPAP yielded superior outcomes to hand instrumentation in terms of patient comfort and time efficiency.28 Therefore, the aim of the present study was to characterize the physical characteristics of EPAP and to evaluate its influence on the clinical and microbiologic parameters over a period of 6 months in patients undergoing SPT.
METHOD AND MATERIALS Study design and ethical approval This examiner-masked, randomized controlled clinical study was conducted at the Department of Periodontology, University of Bern, Switzerland, between September 2010 and March 2012. The study protocol was reviewed and approved by the ethical committee of the Canton Bern, Switzerland (KEK-BE: 109/10). The trial was registered at the German Clinical Trial Register (DRKS: DRKS00005152). Patients received written information about the study and provided written informed consent.
Characterization of material properties of erythritol air-polishing powder Preclinical characterization of the study material was performed at EMS Electro Medical Systems, Nyon, Switzerland. Particle size variation was measured by particle size analysis (Mastersizer 2000, Malvern instruments) and visually checked by scanning electron microscopy (XL-30 FEG, Philips). Abrasiveness was tested on a den-
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Fig 1 A specially designed nozzle is inserted into the pocket to dispense the low abrasive erythritol-based powder and remove the subgingival biofilm.
Fig 2 Immediately after treatment, bleeding from the pocket can be observed.
tin-like synthetic material PEEK GF30 (polyetheretherketone, 30% glass reinforced; Angst & Pfister) through static instrumentation with an Air-Flow Master Piezon (EMS) operated at maximum pressure for 5 seconds and at a distance of 2 mm in a perpendicular direction and performed 43 times (n = 43). Crater deepness, as shown to be a reproducible parameter for volume abrasion,30 was measured by a comparator (Caryshop 25 mm-0.0001, Cary) equipped with a thin tip in order to enable measurement to the bottom of the crater.
Study site selection
Patient selection From September 2010 to March 2011, patients were invited to participate in the study during their regular SPT visit and upon written consent were screened for eligibility according to the following inclusion criteria: • completion of active treatment for moderate to advanced chronic periodontitis • absence of active periodontal therapy 3 months prior to enrolment • presence of ≥ 2 teeth with a minimum of one BOP+ site with a PPD of ≥ 4 mm. Patients were excluded on the basis of: • any antibiotic therapy within 6 months prior to the study • any indication for an endocarditis prophylaxis • any diagnosis such as chronic bronchitis, asthma, or a compromised immune system • any known hypersensitivity to sugar alcohol (polyol).
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In each patient, a minimum of 2 and a maximum of 10 study sites (BOP+ and PPD of ≥ 4 mm) without the presence of detectable subgingival calculus were selected. Furcation involved sites as well as adjacent test sites were excluded from the study.
Interventions All treatment procedures were performed for all patients without local anesthesia by two experienced operators (PH, TH) trained in the use of the air-polishing device by the manufacturer. All patients were provided with SPT according to a slightly modified protocol at baseline (BL), at 3 months (3M), and at 6 months (6M). Apart from test and control sites, the entire dentition was treated according to the standard of care for SPT: residual sites, which were BOP+ or demonstrated PPD ≥ 4 mm, were treated with SRP to remove all hard and soft deposits. At test sites, erythritol was applied by means of an air-polishing device (EPAP) through a single-use nozzle for 5 seconds (Air-Flow Master with Perio-Flow System, EMS).31 The plastic nozzle was directed into the orifice of the periodontal pocket and ejected the erythritol powder in a perpendicular direction towards the root surface (Figs 1 and 2).21 The control sites were instrumented with hand instruments only. Depending on the location of the pockets, either Gracey curettes 11/12, 13/14 (HuFriedy), the universal curette GX4, or the Goldman-Fox
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Fig 3 At 6 months following therapy, a stable, inflammation-free clinical situation can be observed.
curette GX2 (Deppeler) was used. Instrumentation was performed until the operator felt the surface was smooth and free from all subgingival deposits. The SPT was completed by polishing the clinical crowns with rubber cups and a polishing paste of low abrasiveness (Kerr Hawe Cleanic, Kerr Hawe). If oral hygiene practices were insufficient, patients were motivated and instructed in self-performed plaque control.
Clinical assessments One calibrated examiner (CAR) blinded to the treatment provided assessed PPD, CAL, percentage of plaque, and BOP+ sites at BL and at 6M follow-up using a periodontal probe with a diameter of 0.5 millimeter (UNC 15, Hu-Friedy). Site-specific BOP changes were considered as the primary outcome variable (Fig 3).
Subgingival plaque sampling Subgingival plaque samples were obtained from test and control sites at both BL and 6M follow-up. Subgingival plaque was collected by means of sterile paper points, inserted into the study sites for 30 seconds. Paper points were transferred to vials, placed on ice, and stored at −20°C as soon as possible until further analysis was performed.
Assessment of microbial species DNA was extracted by using the Chelex method.32 For the detection of periodontopathogens, the micro-IDent incl. micro-IDent plus (Hain Lifescience) was used. The microIDent incl. microIDent plus test was used to iden-
34
tify 11 periodontopathogenic bacterial species in two runs. Each PCR amplification was carried out in a reaction volume of 25 μL consisting of 2.5 μL of template DNA and 22.5 μL of reaction mixture containing 17.5 μL of primer–nucleotide mix (microIDent and microIDent plus respectively), 2.5 μL of 10 × PCR buffer, 2.5 μl of 25 mmol/L MgCl2, and 1U Taq polymerase (GoTaq, Promega Corporation). The PCR cycling conditions comprised an initial denaturation step at 95°C for 5 minutes, 10 cycles at 95°C for 30 seconds and at 60°C for 2 minutes, 20 cycles at 95°C for 10 seconds, at 55°C for 30 seconds, and at 72°C for 30 seconds, and a final extension step at 72°C for 10 minutes. The subsequent reverse hybridization was performed according to manufacturer’s instructions. In short, the biotinilated amplicons were denatured and incubated at 45°C with hybridization buffer and strips coated with two control lines and five or six species-specific probes. After PCR products had bound to their respective complementary probe, a highly specific washing step removed any unspecifically bound DNA. Streptavidin-conjugated alkaline phosphatase was added, the samples were washed and hybridization products were visualized by adding a substrate for alkaline phosphatase. Finally, the staining intensity of the strips was used for semi-quantification. Two qualified investigators determined independently the scores: 1. no band (negative) 2. weak band (low load) 3. clear band (moderate load) 4. strong band (high load) 5. very strong band (very high load). Both the reference band and the hybridization controls were used for adjustment.
Safety assessment A continuous safety assessment was performed to record adverse events at every visit by clinical examination and interviewing the patients.
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Q U I N T E S S E N C E I N T E R N AT I O N A L
Volume (%)
Hägi et al
90 80 70 60 50 40 30 20 10 0 0.1
a
Erythritol Glycine
1
10 Particle Size (μm)
b
100
600
c
Fig 4 Particle size distribution for erythritol and glycine revealing smaller particle sizes for erythritol (dv10 = 3 μm; dv50 = 13 μm, dv90 = 31 μm) when compared to glycine (dv10 = 5 μm; dv50 = 20 μm, dv90 = 51 μm).
d
Figs 5a to 5d Scanning electron micrographs of air-polishing powder of glycine (a and b) and erythritol (c and d) at different magnifications confirm the smaller particles for erythritol air-polishing powder.
Randomization
Statistical analysis Student t test was applied to compare the preclinical abrasiveness values for erythritol and glycine. Statistical differences of an unequal distribution of gender, smoking status, and age between the groups in the clinical trial were performed using the chi-square or the Mann-Whitney U test. Site-based data from all clinical parameters were averaged before being analyzed. The Wilcoxon signed rank test was performed for testing between BL and 6M, whereas the Mann-Whitney U test was used for group comparison at BL and 6M. With the microbiologic analysis, Wilcoxon signed rank test was applied for the comparison of significances between BL and 6M. P < .05 was considered as statistically significant.
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25 Crater deepness (μm)
Patients enrolled in the study were allocated by one calibrated examiner (CAR) to either control or test group. By applying the minimization method,33 groups were balanced with respect to gender, age, smoking status, and number of sites with a PPD of ≥ 4 mm.
20 15 10 5 0 Erythritol
Glycine
Fig 6 Graph depicting the crater deepness on PEEK 30 resulting from erythritol or glycine by instrumentation for 5 seconds (mean ± standard deviation; n = 43; P = .21).
RESULTS EPAP Particle size distribution as confirmed by SEM-imaging revealed smaller particle sizes for EPAP when compared to GPAP (Figs 4 and 5). Furthermore, EPAP demonstrated slightly lower levels of abrasiveness; however these did not reach statistical significance (P = .21; Fig 6).
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Table 1
Gender, age, and smoking status among both groups EPAP (test)
SRP (control)
P
Age
55.2 ± 7.97
53.7 ± 10.09
0.26*
Gender (male)
65%
60%
0.74 †
Smoking status
40%
45%
0.75 †
* chi-square test; † Mann-Whitney U test.
Table 2
Mean periodontal parameters at baseline (BL) and 6-month (6M) evaluation Patient-based (P)/site-based (S)
EPAP (test)
SRP (control)
BL ± SEM
6M ± SEM
Pa
BL ± SEM
6M ± SEM
P*
.0064
34.45 ± 4.81
21.78 ± 3.06
.0124
Pl (%)
P
31.95 ± 3.79
20.53 ± 3.86
BOP (%)
P
31.70 ± 2.31
26.11 ± 2.90
.0200
36.45 ± 2.84
27.89 ± 2.52
.0055
PPD (mm)
S
4.46 ± 0.07
3.78 ± 0.13
< .0001
4.65 ± 0.09
3.92 ± 0.15
< .0001
CAL (mm)
S
4.90 ± 0.19
4.43 ± 0.24
.0003
5.07 ± 0.21
4.37 ± 0.26
< .0001
* Wilcoxon signed rank (normal approximation). SEM, standard error of the mean.
Table 3
Number of sites with probing pocket depth 4 mm, 5–6 mm, and 7–8 mm at baseline (BL) and 6-month reevaluation (6M) EPAP (test)
SRP (control)
4 mm
5–6 mm
7–8 mm
4 mm
5–6 mm
7–8 mm
BL
56
35
0
54
37
5
6M
66
22
1
64
19
4
Patient selection
Clinical results
In total, 41 patients agreed to participate in the study. Following written consent, a total of 41 patients were screened for eligibility, of which 40 patients were in accordance with the inclusion and exclusion criteria. They were examined and treated according to the study protocol at BL, 3M, and 6M. Two patients had to be excluded from the study during the monitoring period due to a missing follow-up. Out of 38 patients completing the 6M visit, 89 periodontal sites were assigned to the test group and 87 sites to the control group, respectively. Both test and control groups were equally distributed with respect to gender, age, and smoking status (Table 1).
At BL, full-mouth plaque scores were 31.95 ± 3.79% in the EPAP and 34.45 ± 4.81% in the SRP group, respectively. Significant improvements at the 6M visit were recorded in both groups: EPAP, 20.53 ± 3.86% (P = .0064); SRP, 21.78 ± 3.06% (P = .0124). Patient-based full-mouth BOP% yielded significant improvements in both groups without significant between-group differences at both time points. EPAP: BL, 31.70 ± 2.31%; 6M, 26.11 ± 2.90% (P = .02); SRP: BL, 36.45 ± 2.84%; 6M, 27.89 ± 2.52 (P = .0055).
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Primary outcome variable In both groups, BOP levels at study sites decreased from 100% to 40.45% for EPAP and to 42.53% for SRP,
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* * 100
100 EPAP
SRP
EPAP 80 Site Level PI (%)
Site Level BOP (%)
80
SRP
60 40 20
60 40 20
0
0 BL
6M
BL
6M
Fig 7 Site-level percentage of BOP+ sites significantly decreased for both groups between baseline (BL) and the 6-month reevaluation (6M) (mean ± standard deviation; *P < .0001; Wilcoxon signed rank test). EPAP, erythritol powder air-polishing (test); SRP, scaling and root planing (control).
Fig 8 Site-level percentage of Plaque Index (PI%) for both groups between baseline (BL) and the 6-month reevaluation (6M) reveals no difference between groups and time-points (mean + standard deviation; Wilcoxon signed rank test). EPAP, erythritol powder air-polishing (test); SRP, scaling and root planing (control).
respectively (P < .0001). No statistically significant difference was found at the follow-up appointment between the two groups (Fig 7).
quantities at 6M in comparison with BL in both groups. The microbiologic samples positive for 11 species and with a high bacterial load are presented in Table 4.
Secondary outcome variables
Safety and comfort assessment
The assessment of PPD and CAL at the study sites revealed significant improvements for both test and control treatments between BL and the 6M visit (Tables 2 and 3). However, no statistically significant differences were found for site-specific PPD and CAL at both time points for group comparisons (P > .05). Study site evaluation of the Plaque Index excluded a possible bias from an unequal distribution of plaque between test and control sites (Fig 8).
No adverse events were observed or reported with any of the treatment procedures.
Microbiologic assessments The counts of the periodontopathogens Aggregatibacter actinomycetemcomitans, P. gingivalis, Tannerella forsythia, and Treponema denticola did not change significantly during therapy either in the test or in the control group. The counts of Poliana micra were always higher in the control group than in the test group with no significant changes over time. The counts of Eikenella corrodens were higher in the control group at BL. Capnocytophaga species were found in higher
VOLUME 46 • NUMBER 1 • JANUARY 2015
DISCUSSION The present study compared clinically and microbiologically the outcomes following subgingival air polishing with EPAP to SRP by means of hand instruments in patients undergoing SPT. The results failed to reveal any statistically significant differences in the evaluated clinical and microbiologic parameters over the entire study period of 6 months. The preclinical characterization of the study material, however, revealed a slightly lower abrasiveness and smaller particle size for EPAP compared to those reported for GPAP. These findings, coupled with the fact that there were no adverse events related to either treatment modality, indicate that erythritol powder may be a valuable alternative to both glycine powder and hand instruments in patients
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Table 4a Detection of different species by semiquantitative nucleic acid technology for EPAP-treated test sites BL (n = 20) Species Actinomyces actinomycesmcomitans Porphyromonas gingivalis
Positive
6M (n = 19)
High load
Positive
High load
P*, BL–6M
1 (5%)
1 (5%)
1 (5%)
1 (5%)
1.000
13 (65%)
12 (60%)
12 (63%)
10 (53%)
.484
Prevotella intermedia
5 (25%)
4 (20%)
4 (21%)
4 (21%)
.655
Tannerella forsythia
19 (95%)
13 (65%)
15 (79%)
7 (37%)
.381
Treponema denticola
10 (50%)
2 (10%)
11 (58%)
3 (16%)
.553
Poliana micra
12 (60%)
2 (10%)
11 (58%)
1 (5%)
.917
Fusobacterium nucleatum/periodontium
20 (100%)
12 (60%)
18 (95%)
17 (89%)
.144
Campylobacter rectus
18 (90%)
12 (60%)
14 (74%)
11 (58%)
.506
Eubacterium nodatum
6 (30%)
1 (5%)
7 (37%)
1 (5%)
.739
Eikenella corrodens Capnocytophaga species
7 (35%)
1 (5%)
12 (63%)
1 (5%)
.050
10 (50%)
4 (20%)
15 (79%)
11 (58%)
.020
*Wilcoxon test. BL, baseline; 6M, 6-month reevaluation.
Table 4b Detection of different species by semiquantitative nucleic acid technology for SRP-treated test sites BL (n = 20) Species Actinomyces actinomycesmcomitans Porphyromonas gingivalis
6M (n = 20) P*, BL–6M
Positive
High load
Positive
High load
3 (15%)
3 (15%)
4 (20%)
3 (15%)
.715
11 (55%)
10 (50%)
11 (55%)
8 (40%)
.812
Prevotella intermedia
5 (25%)
3 (15%)
4 (20%)
1 (5%)
.550
Tannerella forsythia
15 (75%)
13 (65%)
14 (70%)
12 (60%)
.748
Treponema denticola
10 (50%)
2 (10%)
9 (45%)
0 (0%)
.546
Poliana micra
19 (95%)
12 (60%)
16 (80%)
7 (35%)
.068
Fusobacterium nucleatum/periodontium
20 (100%)
16 (80%)
20 (100%)
17 (85%)
.360
Campylobacter rectus
17 (85%)
11 (55%)
17 (85%)
10 (50%)
.368
Eubacterium nodatum
8 (40%)
3 (15%)
2 (10%)
0 (0%)
.048
Eikenella corrodens
14 (70%)
5 (25%)
15 (65%)
2 (10%)
.859
Capnocytophaga species
10 (50%)
4 (20%)
17 (85%)
4 (20%)
.035
*Wilcoxon test. BL, baseline; 6M, 6-month reevaluation.
with an indication for the removal of supra- and subgingival soft deposits. Based on the fact that short-term studies presented encouraging clinical results with respect to the efficacy of subgingival air polishing,20-22,28 the aim of the present study was to evaluate the new air-polishing powder erythritol for the use in SPT and to further extend the observation period.
38
In contrast to previously published studies20,21 mainly focusing on the qualitative and quantitative analysis of microbiologic changes after EPAP application, the primary outcome variable of the present study was BOP. When considering lowering the risks for periodontal disease progression or tooth loss over longterm, BOP and residual PPD ≥ 6 mm seem to be specific parameters for risk analysis.34 Therefore, a repeated
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Table 4c Comparison of the two groups at specific time-points P* Species
BL
6M
Actinomyces actinomycesmcomitans
0.620
0.461
Porphyromonas gingivalis
0.398
0.627
Prevotella intermedia
0.925
0.813
Tannerella forsythia
0.547
0.667
Treponema denticola
0.862
0.296
Poliana micra
PERIODONTOLOGY
Tobias T. Hägi
The effects of erythritol air-polishing powder on microbiologic and clinical outcomes during supportive periodontal therapy: Six-month results of a randomized controlled clinical trial Tobias T. Hägi, Dr Med Dent1/Petra Hofmänner, Dr Med Dent, MAS2/Sigrun Eick, PD Dr Med Dent2/ Marcel Donnet, PhD 3/Giovanni E. Salvi, Prof Dr Med Dent 4/Anton Sculean, Prof Dr Med Dent, MS, Dr hc5/Christoph A. Ramseier, Dr Med Dent, MAS6 Objectives: To characterize the physical characteristics of a new low abrasive erythritol powder (EPAP) and to evaluate its influence on the clinical and microbiologic parameters over a period of 6 months in patients undergoing supportive periodontal therapy (SPT). Method and Materials: Prior to the clinical application, the particle size and abrasion level of EPAP were compared to glycine air-polishing powder (GPAP) ex vivo. Subsequently, 40 chronic periodontitis patients previously enrolled in SPT were randomly assigned into two groups for the treatment with subgingival EPAP or repeated scaling and root planing (SRP). At baseline (BL), bleeding on probing positive (BOP+) sites with probing pocket depth (PPD) of ≥ 4 mm but no detectable calculus were defined as study sites. During SPT, these sites were either treated by EPAP or SRP at BL, 3, and 6 months (3M, 6M). When indicated, additional SRP was provided. Plaque Index, BOP, PPD, clinical attachment level (CAL), and
subgingival plaque were evaluated at BL and 6M. Results: EPAP yielded lower abrasiveness and smaller particle sizes when compared to GPAP. In 38 patients completing the study, EPAP and SRP resulted in significant reductions of BOP% (EPAP, 40.45%; SRP, 42.53%), PPD (EPAP, -0.67; SRP, -0.68), and increase of CAL (EPAP, 0.48; SRP, 0.61) while at 6M no statistically significant between-group differences were observed (P > .05). Microbiologic evaluation revealed minor shifts in the composition of the subgingival biofilm without influence on periodontopathogenic bacteria. Conclusion: The subgingival use of EPAP by means of an air-polishing device may be considered safe and may lead to comparable clinical and microbiologic outcomes to those obtained with SRP. Clinical Relevance: The subgingival use of EPAP appears to represent a promising modality for the removal of subgingival biofilm during SPT. (Quintessence Int 2015;46:31–41; doi: 10.3290/j.qi.a32817)
Key words: air polishing, bleeding on probing, erythritol, hard tissue loss, supportive periodontal therapy
1
Postgraduate Student, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
5
Professor and Chairman, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
2
Associate Professor and Head of Oral Microbiology Laboratory, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
6
Assistant Professor, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
3
Researcher, EMS Electro Medical System, Nyon, Switzerland.
4
Associate Professor, Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland.
VOLUME 46 • NUMBER 1 • JANUARY 2015
Correspondence: Prof Anton Sculean, Freiburgstrasse 7, 3012 Bern, Switzerland. Email: [email protected]
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The majority of longitudinal clinical studies in periodontal research confirm the significance of supportive periodontal therapy (SPT) for the maintenance of periodontal health.1-5 Well-established treatment protocols for SPT include:6-9 • repeated scaling and root planing (SRP) in periodontal sites with remaining signs of periodontitis (ie, bleeding on probing positive [BOP+] and periodontal pocket depth [PPD] ≥ 4 mm) • debridement of all areas with detectable soft and hard deposits • motivation of the patient to improve their daily selfperformed plaque control. SRP is traditionally performed using metal curettes or sonic/ultrasonic devices, both presenting a comparable outcome.10,11 However, SRP by hand instrumentation or ultrasonic devices need to be performed carefully as their frequent use may lead to dental hard tissue loss.12-18 The introduction of an air-polishing device using glycine air-polishing powder (GPAP) for the removal of supraand subgingival biofilm has been shown to result in less dental hard tissue loss and greater reductions of colony forming units in pockets with 3 to 5 mm PPD compared to the treatment with hand instruments.19 Moreover, no significant differences were found between SRP or ultrasonic instrumentation and GPAP in periodontal pockets on a short-20 and mid-term basis.21,22 The abrasiveness of glycine powder was further demonstrated to be approximately 80% lower than the bicarbonate air-polishing powder previously used.23-26 The latest development of a specially designed nozzle for subgingival air-polishing devices led to a reduction of the working pressure along with an air jet directed perpendicularly to the root surface.20-22 Since none of the published studies reported any adverse events related to the use of subgingival airpolishing devices, it was suggested that for the removal of supra- and subgingival dental biofilms this treatment regime may be superior to hand instrumentation, particularly with respect to patient comfort, dental hard tissue loss, and time efficiency. Recently, a new low abrasive erythritol powder (EPAP) with comparable physical properties to GPAP
32
was introduced for subgingival air polishing. Erythritol, a non-toxic, chemically neutral, and completely watersoluble polyol is widely used as an artificial sweetener and as a food additive.27 Due to its comparable particle size to that of glycine and its promising chemical characteristics allowing the binding of antiseptic substances, it was recently suggested to be suitable for subgingival biofilm removal.28 Additionally, recently published data demonstrated an inhibitory effect of erythritol to some periodontopathogenic bacteria such as Porphyromonas gingivalis.29 Very recent data indicate that subgingival air polishing with EPAP resulted in short-term clinical outcomes comparable to SRP. Moreover, the use of EPAP yielded superior outcomes to hand instrumentation in terms of patient comfort and time efficiency.28 Therefore, the aim of the present study was to characterize the physical characteristics of EPAP and to evaluate its influence on the clinical and microbiologic parameters over a period of 6 months in patients undergoing SPT.
METHOD AND MATERIALS Study design and ethical approval This examiner-masked, randomized controlled clinical study was conducted at the Department of Periodontology, University of Bern, Switzerland, between September 2010 and March 2012. The study protocol was reviewed and approved by the ethical committee of the Canton Bern, Switzerland (KEK-BE: 109/10). The trial was registered at the German Clinical Trial Register (DRKS: DRKS00005152). Patients received written information about the study and provided written informed consent.
Characterization of material properties of erythritol air-polishing powder Preclinical characterization of the study material was performed at EMS Electro Medical Systems, Nyon, Switzerland. Particle size variation was measured by particle size analysis (Mastersizer 2000, Malvern instruments) and visually checked by scanning electron microscopy (XL-30 FEG, Philips). Abrasiveness was tested on a den-
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Fig 1 A specially designed nozzle is inserted into the pocket to dispense the low abrasive erythritol-based powder and remove the subgingival biofilm.
Fig 2 Immediately after treatment, bleeding from the pocket can be observed.
tin-like synthetic material PEEK GF30 (polyetheretherketone, 30% glass reinforced; Angst & Pfister) through static instrumentation with an Air-Flow Master Piezon (EMS) operated at maximum pressure for 5 seconds and at a distance of 2 mm in a perpendicular direction and performed 43 times (n = 43). Crater deepness, as shown to be a reproducible parameter for volume abrasion,30 was measured by a comparator (Caryshop 25 mm-0.0001, Cary) equipped with a thin tip in order to enable measurement to the bottom of the crater.
Study site selection
Patient selection From September 2010 to March 2011, patients were invited to participate in the study during their regular SPT visit and upon written consent were screened for eligibility according to the following inclusion criteria: • completion of active treatment for moderate to advanced chronic periodontitis • absence of active periodontal therapy 3 months prior to enrolment • presence of ≥ 2 teeth with a minimum of one BOP+ site with a PPD of ≥ 4 mm. Patients were excluded on the basis of: • any antibiotic therapy within 6 months prior to the study • any indication for an endocarditis prophylaxis • any diagnosis such as chronic bronchitis, asthma, or a compromised immune system • any known hypersensitivity to sugar alcohol (polyol).
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In each patient, a minimum of 2 and a maximum of 10 study sites (BOP+ and PPD of ≥ 4 mm) without the presence of detectable subgingival calculus were selected. Furcation involved sites as well as adjacent test sites were excluded from the study.
Interventions All treatment procedures were performed for all patients without local anesthesia by two experienced operators (PH, TH) trained in the use of the air-polishing device by the manufacturer. All patients were provided with SPT according to a slightly modified protocol at baseline (BL), at 3 months (3M), and at 6 months (6M). Apart from test and control sites, the entire dentition was treated according to the standard of care for SPT: residual sites, which were BOP+ or demonstrated PPD ≥ 4 mm, were treated with SRP to remove all hard and soft deposits. At test sites, erythritol was applied by means of an air-polishing device (EPAP) through a single-use nozzle for 5 seconds (Air-Flow Master with Perio-Flow System, EMS).31 The plastic nozzle was directed into the orifice of the periodontal pocket and ejected the erythritol powder in a perpendicular direction towards the root surface (Figs 1 and 2).21 The control sites were instrumented with hand instruments only. Depending on the location of the pockets, either Gracey curettes 11/12, 13/14 (HuFriedy), the universal curette GX4, or the Goldman-Fox
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Fig 3 At 6 months following therapy, a stable, inflammation-free clinical situation can be observed.
curette GX2 (Deppeler) was used. Instrumentation was performed until the operator felt the surface was smooth and free from all subgingival deposits. The SPT was completed by polishing the clinical crowns with rubber cups and a polishing paste of low abrasiveness (Kerr Hawe Cleanic, Kerr Hawe). If oral hygiene practices were insufficient, patients were motivated and instructed in self-performed plaque control.
Clinical assessments One calibrated examiner (CAR) blinded to the treatment provided assessed PPD, CAL, percentage of plaque, and BOP+ sites at BL and at 6M follow-up using a periodontal probe with a diameter of 0.5 millimeter (UNC 15, Hu-Friedy). Site-specific BOP changes were considered as the primary outcome variable (Fig 3).
Subgingival plaque sampling Subgingival plaque samples were obtained from test and control sites at both BL and 6M follow-up. Subgingival plaque was collected by means of sterile paper points, inserted into the study sites for 30 seconds. Paper points were transferred to vials, placed on ice, and stored at −20°C as soon as possible until further analysis was performed.
Assessment of microbial species DNA was extracted by using the Chelex method.32 For the detection of periodontopathogens, the micro-IDent incl. micro-IDent plus (Hain Lifescience) was used. The microIDent incl. microIDent plus test was used to iden-
34
tify 11 periodontopathogenic bacterial species in two runs. Each PCR amplification was carried out in a reaction volume of 25 μL consisting of 2.5 μL of template DNA and 22.5 μL of reaction mixture containing 17.5 μL of primer–nucleotide mix (microIDent and microIDent plus respectively), 2.5 μL of 10 × PCR buffer, 2.5 μl of 25 mmol/L MgCl2, and 1U Taq polymerase (GoTaq, Promega Corporation). The PCR cycling conditions comprised an initial denaturation step at 95°C for 5 minutes, 10 cycles at 95°C for 30 seconds and at 60°C for 2 minutes, 20 cycles at 95°C for 10 seconds, at 55°C for 30 seconds, and at 72°C for 30 seconds, and a final extension step at 72°C for 10 minutes. The subsequent reverse hybridization was performed according to manufacturer’s instructions. In short, the biotinilated amplicons were denatured and incubated at 45°C with hybridization buffer and strips coated with two control lines and five or six species-specific probes. After PCR products had bound to their respective complementary probe, a highly specific washing step removed any unspecifically bound DNA. Streptavidin-conjugated alkaline phosphatase was added, the samples were washed and hybridization products were visualized by adding a substrate for alkaline phosphatase. Finally, the staining intensity of the strips was used for semi-quantification. Two qualified investigators determined independently the scores: 1. no band (negative) 2. weak band (low load) 3. clear band (moderate load) 4. strong band (high load) 5. very strong band (very high load). Both the reference band and the hybridization controls were used for adjustment.
Safety assessment A continuous safety assessment was performed to record adverse events at every visit by clinical examination and interviewing the patients.
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Volume (%)
Hägi et al
90 80 70 60 50 40 30 20 10 0 0.1
a
Erythritol Glycine
1
10 Particle Size (μm)
b
100
600
c
Fig 4 Particle size distribution for erythritol and glycine revealing smaller particle sizes for erythritol (dv10 = 3 μm; dv50 = 13 μm, dv90 = 31 μm) when compared to glycine (dv10 = 5 μm; dv50 = 20 μm, dv90 = 51 μm).
d
Figs 5a to 5d Scanning electron micrographs of air-polishing powder of glycine (a and b) and erythritol (c and d) at different magnifications confirm the smaller particles for erythritol air-polishing powder.
Randomization
Statistical analysis Student t test was applied to compare the preclinical abrasiveness values for erythritol and glycine. Statistical differences of an unequal distribution of gender, smoking status, and age between the groups in the clinical trial were performed using the chi-square or the Mann-Whitney U test. Site-based data from all clinical parameters were averaged before being analyzed. The Wilcoxon signed rank test was performed for testing between BL and 6M, whereas the Mann-Whitney U test was used for group comparison at BL and 6M. With the microbiologic analysis, Wilcoxon signed rank test was applied for the comparison of significances between BL and 6M. P < .05 was considered as statistically significant.
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25 Crater deepness (μm)
Patients enrolled in the study were allocated by one calibrated examiner (CAR) to either control or test group. By applying the minimization method,33 groups were balanced with respect to gender, age, smoking status, and number of sites with a PPD of ≥ 4 mm.
20 15 10 5 0 Erythritol
Glycine
Fig 6 Graph depicting the crater deepness on PEEK 30 resulting from erythritol or glycine by instrumentation for 5 seconds (mean ± standard deviation; n = 43; P = .21).
RESULTS EPAP Particle size distribution as confirmed by SEM-imaging revealed smaller particle sizes for EPAP when compared to GPAP (Figs 4 and 5). Furthermore, EPAP demonstrated slightly lower levels of abrasiveness; however these did not reach statistical significance (P = .21; Fig 6).
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Table 1
Gender, age, and smoking status among both groups EPAP (test)
SRP (control)
P
Age
55.2 ± 7.97
53.7 ± 10.09
0.26*
Gender (male)
65%
60%
0.74 †
Smoking status
40%
45%
0.75 †
* chi-square test; † Mann-Whitney U test.
Table 2
Mean periodontal parameters at baseline (BL) and 6-month (6M) evaluation Patient-based (P)/site-based (S)
EPAP (test)
SRP (control)
BL ± SEM
6M ± SEM
Pa
BL ± SEM
6M ± SEM
P*
.0064
34.45 ± 4.81
21.78 ± 3.06
.0124
Pl (%)
P
31.95 ± 3.79
20.53 ± 3.86
BOP (%)
P
31.70 ± 2.31
26.11 ± 2.90
.0200
36.45 ± 2.84
27.89 ± 2.52
.0055
PPD (mm)
S
4.46 ± 0.07
3.78 ± 0.13
< .0001
4.65 ± 0.09
3.92 ± 0.15
< .0001
CAL (mm)
S
4.90 ± 0.19
4.43 ± 0.24
.0003
5.07 ± 0.21
4.37 ± 0.26
< .0001
* Wilcoxon signed rank (normal approximation). SEM, standard error of the mean.
Table 3
Number of sites with probing pocket depth 4 mm, 5–6 mm, and 7–8 mm at baseline (BL) and 6-month reevaluation (6M) EPAP (test)
SRP (control)
4 mm
5–6 mm
7–8 mm
4 mm
5–6 mm
7–8 mm
BL
56
35
0
54
37
5
6M
66
22
1
64
19
4
Patient selection
Clinical results
In total, 41 patients agreed to participate in the study. Following written consent, a total of 41 patients were screened for eligibility, of which 40 patients were in accordance with the inclusion and exclusion criteria. They were examined and treated according to the study protocol at BL, 3M, and 6M. Two patients had to be excluded from the study during the monitoring period due to a missing follow-up. Out of 38 patients completing the 6M visit, 89 periodontal sites were assigned to the test group and 87 sites to the control group, respectively. Both test and control groups were equally distributed with respect to gender, age, and smoking status (Table 1).
At BL, full-mouth plaque scores were 31.95 ± 3.79% in the EPAP and 34.45 ± 4.81% in the SRP group, respectively. Significant improvements at the 6M visit were recorded in both groups: EPAP, 20.53 ± 3.86% (P = .0064); SRP, 21.78 ± 3.06% (P = .0124). Patient-based full-mouth BOP% yielded significant improvements in both groups without significant between-group differences at both time points. EPAP: BL, 31.70 ± 2.31%; 6M, 26.11 ± 2.90% (P = .02); SRP: BL, 36.45 ± 2.84%; 6M, 27.89 ± 2.52 (P = .0055).
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Primary outcome variable In both groups, BOP levels at study sites decreased from 100% to 40.45% for EPAP and to 42.53% for SRP,
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* * 100
100 EPAP
SRP
EPAP 80 Site Level PI (%)
Site Level BOP (%)
80
SRP
60 40 20
60 40 20
0
0 BL
6M
BL
6M
Fig 7 Site-level percentage of BOP+ sites significantly decreased for both groups between baseline (BL) and the 6-month reevaluation (6M) (mean ± standard deviation; *P < .0001; Wilcoxon signed rank test). EPAP, erythritol powder air-polishing (test); SRP, scaling and root planing (control).
Fig 8 Site-level percentage of Plaque Index (PI%) for both groups between baseline (BL) and the 6-month reevaluation (6M) reveals no difference between groups and time-points (mean + standard deviation; Wilcoxon signed rank test). EPAP, erythritol powder air-polishing (test); SRP, scaling and root planing (control).
respectively (P < .0001). No statistically significant difference was found at the follow-up appointment between the two groups (Fig 7).
quantities at 6M in comparison with BL in both groups. The microbiologic samples positive for 11 species and with a high bacterial load are presented in Table 4.
Secondary outcome variables
Safety and comfort assessment
The assessment of PPD and CAL at the study sites revealed significant improvements for both test and control treatments between BL and the 6M visit (Tables 2 and 3). However, no statistically significant differences were found for site-specific PPD and CAL at both time points for group comparisons (P > .05). Study site evaluation of the Plaque Index excluded a possible bias from an unequal distribution of plaque between test and control sites (Fig 8).
No adverse events were observed or reported with any of the treatment procedures.
Microbiologic assessments The counts of the periodontopathogens Aggregatibacter actinomycetemcomitans, P. gingivalis, Tannerella forsythia, and Treponema denticola did not change significantly during therapy either in the test or in the control group. The counts of Poliana micra were always higher in the control group than in the test group with no significant changes over time. The counts of Eikenella corrodens were higher in the control group at BL. Capnocytophaga species were found in higher
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DISCUSSION The present study compared clinically and microbiologically the outcomes following subgingival air polishing with EPAP to SRP by means of hand instruments in patients undergoing SPT. The results failed to reveal any statistically significant differences in the evaluated clinical and microbiologic parameters over the entire study period of 6 months. The preclinical characterization of the study material, however, revealed a slightly lower abrasiveness and smaller particle size for EPAP compared to those reported for GPAP. These findings, coupled with the fact that there were no adverse events related to either treatment modality, indicate that erythritol powder may be a valuable alternative to both glycine powder and hand instruments in patients
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Table 4a Detection of different species by semiquantitative nucleic acid technology for EPAP-treated test sites BL (n = 20) Species Actinomyces actinomycesmcomitans Porphyromonas gingivalis
Positive
6M (n = 19)
High load
Positive
High load
P*, BL–6M
1 (5%)
1 (5%)
1 (5%)
1 (5%)
1.000
13 (65%)
12 (60%)
12 (63%)
10 (53%)
.484
Prevotella intermedia
5 (25%)
4 (20%)
4 (21%)
4 (21%)
.655
Tannerella forsythia
19 (95%)
13 (65%)
15 (79%)
7 (37%)
.381
Treponema denticola
10 (50%)
2 (10%)
11 (58%)
3 (16%)
.553
Poliana micra
12 (60%)
2 (10%)
11 (58%)
1 (5%)
.917
Fusobacterium nucleatum/periodontium
20 (100%)
12 (60%)
18 (95%)
17 (89%)
.144
Campylobacter rectus
18 (90%)
12 (60%)
14 (74%)
11 (58%)
.506
Eubacterium nodatum
6 (30%)
1 (5%)
7 (37%)
1 (5%)
.739
Eikenella corrodens Capnocytophaga species
7 (35%)
1 (5%)
12 (63%)
1 (5%)
.050
10 (50%)
4 (20%)
15 (79%)
11 (58%)
.020
*Wilcoxon test. BL, baseline; 6M, 6-month reevaluation.
Table 4b Detection of different species by semiquantitative nucleic acid technology for SRP-treated test sites BL (n = 20) Species Actinomyces actinomycesmcomitans Porphyromonas gingivalis
6M (n = 20) P*, BL–6M
Positive
High load
Positive
High load
3 (15%)
3 (15%)
4 (20%)
3 (15%)
.715
11 (55%)
10 (50%)
11 (55%)
8 (40%)
.812
Prevotella intermedia
5 (25%)
3 (15%)
4 (20%)
1 (5%)
.550
Tannerella forsythia
15 (75%)
13 (65%)
14 (70%)
12 (60%)
.748
Treponema denticola
10 (50%)
2 (10%)
9 (45%)
0 (0%)
.546
Poliana micra
19 (95%)
12 (60%)
16 (80%)
7 (35%)
.068
Fusobacterium nucleatum/periodontium
20 (100%)
16 (80%)
20 (100%)
17 (85%)
.360
Campylobacter rectus
17 (85%)
11 (55%)
17 (85%)
10 (50%)
.368
Eubacterium nodatum
8 (40%)
3 (15%)
2 (10%)
0 (0%)
.048
Eikenella corrodens
14 (70%)
5 (25%)
15 (65%)
2 (10%)
.859
Capnocytophaga species
10 (50%)
4 (20%)
17 (85%)
4 (20%)
.035
*Wilcoxon test. BL, baseline; 6M, 6-month reevaluation.
with an indication for the removal of supra- and subgingival soft deposits. Based on the fact that short-term studies presented encouraging clinical results with respect to the efficacy of subgingival air polishing,20-22,28 the aim of the present study was to evaluate the new air-polishing powder erythritol for the use in SPT and to further extend the observation period.
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In contrast to previously published studies20,21 mainly focusing on the qualitative and quantitative analysis of microbiologic changes after EPAP application, the primary outcome variable of the present study was BOP. When considering lowering the risks for periodontal disease progression or tooth loss over longterm, BOP and residual PPD ≥ 6 mm seem to be specific parameters for risk analysis.34 Therefore, a repeated
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Table 4c Comparison of the two groups at specific time-points P* Species
BL
6M
Actinomyces actinomycesmcomitans
0.620
0.461
Porphyromonas gingivalis
0.398
0.627
Prevotella intermedia
0.925
0.813
Tannerella forsythia
0.547
0.667
Treponema denticola
0.862
0.296
Poliana micra
