Clinical and Immunological Effects of Er,Cr:YSGG Laser in Nonsurgical Periodontal Treatment: A Randomized Clinical Trial

Abstract

Objective:

The aim of this study was to compare the clinical and immunological results of nonsurgical periodontal treatment with or without the erbium, chromium:yttrium–scandium–gallium–garnet (Er,Cr:YSGG) laser.

Background data:

As lasers have begun to be used in dentistry, the Er,Cr:YSGG laser has started to attract attention in the field of periodontology.

Materials and methods:

Fifty-nine nonsmoking patients with advanced chronic periodontitis were randomly allocated to a test group (full-mouth ultrasonic supra- and subgingival debridement+Er,Cr:YSGG laser application) and a control group (full-mouth ultrasonic supra- and subgingival debridement+root planing with Gracey curettes). The laser parameters were set as follows: 1.5 W output power, pulse mode H (pulse duration of 140 μs), pulse frequency of 20 Hz, and an air–water spray ratio of 10% air and 15% water. The instrumentation was performed until the operator felt that the root surfaces were adequately debrided. Probing depth (PD), clinical attachment level (CAL), bleeding on probing (BOP), plaque index, interleukin-1 beta (IL-1β), matrix metalloproteinase-8 (MMP-8), tissue inhibitor metalloproteinase-1 (TIMP-1), and MMP-8/TIMP-1 levels in gingival crevicular fluid were evaluated at baseline, 6 weeks, and 3 months postoperatively.

Results:

There were statistically significant differences in PD, which was our primary outcome, and BOP between the groups at both examinations [p < 0.001 and p < 0.001 (for PD) and p = 0.048 and p < 0.001 (for BOP), respectively], in favor of the laser group. However, there were no significant differences among groups at any time for CAL gain (p = 563 and p = 369, respectively). No significant differences in MMP-8, TIMP-1, and MMP-8/TIMP-1 levels were detected among groups. There was a statistically significant difference for IL-1β levels among groups at 3-month evaluations in favor of the laser group.

Conclusions:

Using the Er,Cr:YSGG laser instead of hand instruments in nonsurgical periodontal treatment has shown additional improvements in terms of pocket reduction and gingival bleeding compared with traditional nonsurgical therapy.

Introduction

Periodontitis is an inflammatory disease resulting in breakdown of the periodontal tissues in susceptible patients.¹ The primary aim of periodontal treatment is to achieve a biocompatible root surface by removing bacterial biofilms, calculus, and the smear layer, which is traditionally performed by hand instruments or sonic and ultrasonic scalers.^2

–5 However, limitations of these tools evoke a search for new methods in nonsurgical periodontal therapy.⁶ In addition, root planing with Gracey curettes results in a smear layer, which may have a negative effect on healing.^7
–9

In recent years, treatment by different types of lasers such as erbium-doped:yttrium, aluminum, and garnet (Er:YAG), erbium, chromium:yttrium–scandium–gallium–garnet (Er,Cr:YSGG), neodymium-doped yttrium aluminum garnet (Nd:YAG), and diode laser has been proposed as an alternative or adjunct to initial periodontal treatment because of its photobiomodulation, bactericidal, and antifungal effects.^{6,10

–19} Er:YAG (wavelength 2940 nm) and Er,Cr:YSGG (wavelength 2790 nm) lasers have been claimed to be effective tools for root debridement with no adverse thermal effects, especially in sites where traditional hand instruments cannot reach.^20,21

Since root debridement with ultrasonic devices and hand instruments results in the smear layer and unneeded removal of cementum, the Er,Cr:YSGG laser could be used as an alternative to conventional methods without any major harm to the tooth.²² While erbium lasers have been compared with traditional, nonsurgical periodontal treatment in previous studies,^{13,15,19,23

–32} there is still a requirement for new studies with Er,Cr:YSGG.

Based on this information, our null hypothesis was that there would be no differences between the laser group and conventional treatment group in terms of clinical and immunological indices.

The aim of this study is to compare the clinical and immunological results of nonsurgical periodontal treatment in nonsmokers using ultrasonic scalers with the Er,Cr:YSGG laser or with hand instruments.

Materials and Methods

The trial was planned as a parallel, randomized, and controlled test over a 3-month period. The study protocol was approved by the Republic of Turkey Bezmialem University's Clinical Research Ethics Committee with the permit number 17551, and informed consent forms were collected from each participant. The study was registered under the International Clinical Trials Registry Platform with the Thai Clinical Trials Registry TCTR20180123001.

After periodontal and radiographic evaluation from January 2016 to July 2016, the advanced chronic periodontitis patients who meet the following criteria were asked to attend the study: (1) having >3 teeth in each quadrant; (2) having at least four periodontal pockets with a probing depth (PD) of ≥5 mm³³; (3) no systemic diseases or medication that can affect the periodontal status; (4) no periodontal treatment in the last 1 year; (5) no antibiotic usage in the last 6 months; (6) no pregnancy, menopause, or breastfeeding; (7) no smoking; and (8) no removable dental prosthesis. Eighty-six patients of 124 met the criteria above and 80 (40 males and 40 females aged between 31 and 56) accepted to join the study.

This multi-center, parallel designed study was conducted in the Periodontology Department of Bezmialem University and in the Periodontology Department of the Istanbul University Faculty of Dentistry. After randomization, the test group received full-mouth subgingival debridement with an ultrasonic device+Er,Cr:YSGG laser (SPL), while the control group received only full-mouth root planing with an ultrasonic device+Gracey curettes (SRP).

All participants received supragingival scaling and oral hygiene instructions 2 weeks before the treatment and the ones who showed plaque scores of >1 were not involved in the study.³⁴ A reinforcement of oral hygiene was performed at all visits.

Allocation of groups was done by opaque sealed envelopes, and assignments were revealed to the operator only on the day the treatment was administered. Patients in the SPL group (n = 30 patients) received full-mouth ultrasonic debridement (LM ProPower, Finland)+Er,Cr:YSGG (Waterlase; Biolase) laser application within 24 h. The parameters of the laser were set as follows: output power of 1.5 W, pulse mode H (pulse duration of 140 μs), pulse frequency of 20 Hz, energy density of 20.77 J/cm², power density of 57.7 W/cm², cumulative dose of 20.77 J/cm², and an air–water ratio of 10% air and 15% water. Fiber tips (Radial Firing Perio Tips; Biolase) of 500 μm diameter and 14 mm length were used. The parameters applied in the study are shown in Table 1.

Table 1.

Parameters of Er,Cr:YSGG Laser

Power density	57.70 W/cm²
Energy density/per point	20.77 J/cm²
Duration of treatment session	20 sec
Frequency of the treatment (per pocket)	1 time
Cumulative dose	20.77 J/cm²

Er,Cr:YSGG, erbium, chromium:yttrium–scandium–gallium–garnet.

Laser application was performed in parallel paths, from coronal to apical direction. The fiber tip was inclined 15–20° to the root surface. The SRP group (n = 29 patients) only received scaling and root planing using an ultrasonic scaler (LM ProPower) and Gracey curettes (Hu-Friedy Co., Chicago, IL).

All the clinical indices were recorded and immunological samplings were collected by an experienced clinician (U.B.) who was blinded to the treatment groups. Treatments were done under local anesthesia. The operator ended the treatment after the root surfaces were sufficiently debrided or planed. Only one experienced operator carried out the treatments (D.E.), and another independent periodontist (K.N.) confirmed the end-points of all the treatments.

The following clinical indices were recorded at all visits: PD, bleeding on probing (BOP),³⁵ and clinical attachment loss (CAL). A Williams periodontal probe (Hu-Friedy Co.) was used to measure the six sites around the teeth (mesio-buccal, mid-buccal, disto-buccal, mesio-lingual/palatal, mid-lingual/palatal, and disto-lingual/palatal). The periodontal probe was placed parallel to the long axis of the tooth when measuring the PD and CAL, which were recorded in millimeters. The examinations were performed at baseline, 6 weeks, and 3 months after treatments.³⁶

PDs were grouped into those between 4 and 6 mm (>3 and <7) and those >6 mm.

A calibration exercise was performed on five randomly selected, advanced chronic periodontitis patients who are not included in the study to determine acceptable intraexaminer reproducibility. The examiner measured PD and BOP scores twice for each patient, on two different days. The mean difference was <0.5 mm for PD. BOP scores were the same for 90% of the measurements. Calibration was accepted if the two measurements were ≥90% consistent with each other.

Sample collection and immunological analysis

Gingival crevicular fluid was collected for immunological analysis at baseline, 6 weeks, and 3 months after treatment from the deepest pockets of single-rooted teeth presenting a maximum of 9-mm PD. Four different samples were obtained from each patient, all from different pockets. After removing plaque, selected teeth were isolated to prevent contamination by saliva.

For sample collection, sterile, absorbent PerioPaper strips (PerioPaper: Oraflow, Inc., NY.) were gently inserted into the pockets for 30 s. The pooled strips for each patient were placed in sterile Eppendorf tubes and stored at −80°C until required. The following parameters were analyzed with ELISA kits (Diaclone SAS, France; R&D Systems, Inc.) according to the manufacturer's instructions: interleukin-1 beta (IL-1β), matrix metalloproteinase-8 (MMP-8), and tissue inhibitor metalloproteinase-1 (TIMP-1). The results were reported as concentration amounts and presented as picograms per milliliter or nanograms per milliliter.

Statistical analysis

The sample size calculation was based on the main outcome variable (PD reduction), α error of 0.05, and β error of 0.20. Thus, the power of the study was calculated to be 80% with a size of 26 patients per group. With the assumption of dropouts (50%), 80 patients were included and randomized.

The statistical analysis was performed using a computer program (MedCalc Statistical Software, version 12.7.7, Ostend, Belgium). The patient was the unit of observation for clinical periodontal analysis. Normal distribution was checked by Student's t and paired sample t-tests. Data that are not distributed normally were checked by the Mann–Whitney U and Wilcoxon signed-rank tests. The level of significance was determined as p < 0.05.

Results

To allow patient dropout throughout the trial, 80 patients were involved. Four patients were excluded from the study because of antibiotic usage (1 from the test group and 3 from the control group), 2 because of developing medical conditions that affect the outcomes of periodontal treatment (2 from the test group), and 15 (7 from the test group and 8 from the control group) were lost to follow-up. Fifty-nine (30 males and 29 females) patients completed the 3-month study period.

Characteristics of the participants are shown in Table 2.

Table 2.

Descriptive Parameters of Study Groups

	Test group	Control group
No. of patients	30	29
Mean age (min/max years) (mean ± SD)	31/56	32/51
Mean age (min/max years) (mean ± SD)	41.03 ± 8.06	39.72 ± 6.16
Female (n, %)	14, 46.70	16, 56.20
Male (n, %)	16, 53.30	13, 44.80

SD, standard deviation.

Clinical assessments

Mean PD, CAL, and BOP values for both treatment groups are reported in Table 3. No significant differences in the above parameters were detected at baseline.

Table 3.

Differences in Clinical Parameters

Parameter, mean ± SD	Baseline (0)	6 Weeks	Difference (0–6 weeks)	p	3 Months	Difference (0–3 months)	p
Bleeding on probing (%)
Test (n = 30)	89 ± 0.07	17 ± 0.09	72 ± 0.11	<0.001	12 ± 0.06	76 ± 0.07	<0.001
Control (n = 29)	86 ± 0.04	19 ± 0.07	66 ± 0.08	<0.001	19 ± 0.06	66 ± 0.06	<0.001
p	0.160	0.065	0.048		<0.001	<0.001
Probing depth (mm)
Test (n = 30)	3.76 ± 0.30	2.50 ± 0.30	1.25 ± 0.18	<0.001	2.41 ± 0.27	1.35 ± 0.20	<0.001
Control (n = 29)	3.91 ± 0.20	2.94 ± 0.29	0.98 ± 0.22	<0.001	2.96 ± 0.30	0.95 ± 0.22	<0.001
p	0.109	<0.001	<0.001		<0.001	<0.001
Clinical attachment level (mm)
Test (n = 30)	3.99 ± 0.50	3.20 ± 0.50	0.76 ± 0.19	<0.001	3.10 ± 0.40	0.88 ± 0.32	<0.001
Control (n = 29)	4.14 ± 0.40	3.29 ± 0.48	0.84 ± 0.22	<0.001	3.30 ± 0.50	0.84 ± 0.22	<0.001
p	0.277	0.461	0.563		0.103	0.369

BOP results showed reduction in both groups independently, with a statistically significant difference in favor of the SPL group by 6 weeks and 3 months (p = 0.048 and p < 0.001, respectively).

Mean PD values in the SPL group showed a statistically significant greater reduction compared with the SRP group at 6-week and 3-month examinations (p < 0.001 and p < 0.001, respectively).

Table 3 demonstrates the mean values of CAL. Both treatment methods resulted in a statistically significant reduction in mean CAL scores at 6 weeks and 3 months post-treatment (p < 0.001 and p < 0.001, respectively), but no statistically significant difference was noted among groups at any time point.

Table 4 shows the mean values of clinical variables at different time points for pockets 4–6 and >6 mm deep. PD scores showed statistically significant improvements in the SPL group compared with the SRP group at all time points for both PDs (for PD 4–6 mm, p < 0.001 and p < 0.001, respectively, and for PD >6 mm, p < 0.001 and p < 0.001, respectively). BOP also showed statistically significant improvements in favor of the test group at all time points for both PDs (for PD 4–6 mm, p < 0.001 and p < 0.001, respectively, and for PD >6 mm, p < 0.001 and p < 0.001, respectively). The SPL group demonstrated significantly more reduction in CAL values than the SRP group for 4- to 6-mm pockets at 3 months control (p < 0.001) and for >6-mm pockets at both time points (p = 0.021 and p < 0.001, respectively).

Table 4.

Means of Clinical Parameters (PD 4–6 mm and PD >6 mm)

Parameter, mean ± SD	PD 4–6 mm			PD >6 mm
Parameter, mean ± SD	Baseline (0)	6 Weeks	3 Months	Baseline (0)	6 Weeks	3 Months
Bleeding on probing (%)
Test (n = 30)	95 ± 0.20	24 ± 0.40	18 ± 0.40	99 ± 0.10	71 ± 0.40	56 ± 0.50
Control (n = 29)	90 ± 0.20	30 ± 0.50	31 ± 0.50	100	90 ± 0.26	89 ± 0.30
p	0.008	<0.001	<0.001	0.139	<0.001	<0.001
Probing depth (mm)
Test (n = 30)	4.70 ± 0.70	2.80 ± 0.70	2.70 ± 0.70	7.50 ± 0.80	4.90 ± 0.90	4.40 ± 0.90
Control (n = 29)	4.70 ± 0.70	3.40 ± 0.70	3.30 ± 0.70	7.50 ± 0.70	5.40 ± 1.10	5.20 ± 1.20
p	0.279	<0.001	<0.001	0.852	<0.001	<0.001
Clinical attachment level (mm)
Test (n = 30)	4.77 ± 1.06	3.67 ± 1.11	3.40 ± 1.07	7.06 ± 1.30	5.80 ± 1.10	5.10 ± 1.20
Control (n = 29)	4.80 ± 0.90	3.70 ± 0.90	3.70 ± 0.90	7.60 ± 1.10	6.10 ± 1.20	5.90 ± 1.30
p	0.202	0.076	<0.001	<0.001	0.021	<0.001

PD, probing depth.

Immunological assessments

IL-1β values showed a statistically significant intragroup difference at both visits. The results showed statistically significant intergroup differences at 6 weeks control (p = 0.002), while showing no significant difference at the 3-month examination (p = 0.304) (Table 5).

Table 5.

Differences in Immunological Parameters

Parameter, mean ± SD	Baseline	6 Weeks	p	3 Months	p
IL-1β (pg/mL)
Test (n = 30)	2621.80 ± 676.90	1378.80 ± 839.70	<0.001	896.30 ± 844.80	<0.001
Control (n = 29)	1671.10 ± 1053.10	767.80 ± 765.30	<0.001	1005.90 ± 719.80	<0.001
p	0.002	0.002		0.304
MMP-8 (ng/mL)
Test (n = 30)	232.20 ± 262.70	53.50 ± 22.30	<0.001	61.07 ± 29.70	<0.001
Control (n = 29)	331.50 ± 299.70	75.03 ± 49.20	<0.001	68.70 ± 60.50	<0.001
p	0.102	0.157		0.578
TIMP-1 (ng/mL)
Test (n = 30)	30.60 ± 3.80	29.90 ± 2.60	0.464	28.60 ± 2.90	0.049
Control (n = 29)	32.05 ± 10.80	28.50 ± 2.90	0.151	32.10 ± 1.90	0.111
p	0.414	0.101		<0.001
MMP-8/TIMP-1
Test (n = 30)	7.30 ± 7.50	1.80 ± 0.80	<0.001	0.10 ± 0.90	<0.001
Control (n = 29)	9.80 ± 7.60	2.70 ± 1.70	<0.001	0.10 ± 1.80	<0.001
p	0.083	0.066		0.274

IL-1β, interleukin-1 beta; MMP-8, matrix metalloproteinase-8; TIMP-1, tissue inhibitor metalloproteinase-1.

MMP-8/TIMP-1 levels showed a statistically significant improvement within both groups (p < 0.001), while no intergroup differences could be noted at any time point (p > 0.05).

Discussion

Previous studies showed that erbium laser therapy either as a monotherapy or as an adjunct to traditional nonsurgical treatment leads to statistically significant advancements in clinical parameters.^{16,25

–28,30,37,38} In a recent literature review, it has been reported that calculus removal using ultrasonic and hand instruments showed remaining calculus, whereas erbium lasers revealed much smaller amounts compared with the traditional methods.³⁰ The aim of this trial was to see the effects of the Er,Cr:YSGG laser in initial periodontal therapy and to compare the short-term results of the two methods. The SPL group showed statistically significant greater improvements in indices such as PD and BOP than the SRP group.

Intragroup comparisons have demonstrated that both methods were efficient in advanced chronic periodontitis patients and resulted in statistically significant reductions in PD, CAL, BOP, IL-1β, and MMP-8 levels at 6 weeks and 3 months after therapy. The result that both methods result in statistically significant improvements in clinical indices within groups is in accordance with previous studies both in Er,Cr:YSGG^{15,31,39
–41} and Er:YAG.^{12,13,23,25,26,28,42}

PD, which is our primary outcome, showed significant results in favor of the SPL group after 3-month evaluations. This is in accordance with results of some earlier studies conducted with the Er:YAG laser.^{12,15,24,26,43} Other studies have reported no significant differences in PD changes among groups.^{13,23,25,27,28,42,44}

As we expected, deep pockets (>6 mm) showed greater reduction in PD values than 4- to 6-mm pockets in both groups, in accordance with previous studies.^{12,23,25,26,36} Less than 6-millimeter pockets showed a statistically significant decrease in PD values compared with 4- to 6-mm pockets at both evaluation periods. Since the efficacy of nonsurgical periodontal treatment is related to the initial PD, and deeper pockets have more potential for PD reduction and CAL gain, this result is not surprising.⁴⁵ In addition, deep pockets are more accessible with the Er,Cr:YSGG laser than hand instruments, which can explain the better healing of the test group in >6-mm pockets.

BOP scores in SPL and SRP groups reduced dramatically, which is in agreement with previously reported data.^{12,15,23

–26,36,42,46} Besides, a statistically significant greater reduction of BOP values was seen in the test group. These results also match with the previous ones.^15,24,26 Krohn-Dale et al. have reported high BOP scores throughout the study.⁴⁴ The investigators reported that this distinct result might be due to tiredness and loss of will power of patients. Schwarz et al.,²⁵ Sculean et al.,²³ Lopes et al.,^27,28 Sanz-Sánchez et al.,¹⁴ and Ratka-Krüger et al.⁴² could not find any significant differences among groups in terms of BOP reduction, while Soo et al.³⁶ reported that both protocols led to a reduction in BOP, with a statistically significant greater reduction in the SRP group.

In addition, deeper pockets showed less reduction than moderate pockets in our study in terms of BOP.

The Er,Cr:YSGG laser showed a similar CAL gain when compared with the test group. Sculean et al.,²³ Tomasi et al.,⁴³ Rotundo et al.,⁴⁷ Lopes et al.,²⁸ Ratka-Krüger et al.,⁴² Sanz-Sánchez et al.,¹³ and Schwarz et al.²⁵ reported similar results to the present study in terms of CAL gain.

Conversely, Crespi et al.,¹² in a randomized controlled study, reported that the CAL gain was higher in the laser group. In addition, Schwarz et al.^24,26 and Kelbauskiene et al.¹⁵ also observed a significantly higher CAL gain in laser-treated sites compared with the SRP group. They applied root planing with Gracey curettes to both groups, while we only applied subgingival scaling with ultrasonic scalers to the control group. That is why it would not be surprising that CAL gain showed a statistically significant improvement in favor of the SRP+Er,Cr:YSGG group to which two different procedures were applied.

Lopes et al.²⁷ and Soo et al.,³⁶ comparing Er:YAG laser and SRP, reported that the SRP group showed a statistically significant CAL gain compared with the laser group. Lopes et al. reported that the laser group did not show a statistically significant difference in CAL values, which might be due to a short evaluation period (30 days).³⁶ Deep pockets (>6 mm) showed greater reduction in CAL values than 4- to 6-mm pockets, as in other previous studies.^{12,23,25,26,36}

In this particular study, clinical results and the effective control of inflammation with both treatment methods may explain the reduction in immunological markers within groups, especially in IL-1β levels. Lopes et al. have reported in a randomized controlled trial that IL-1β levels did not show any significant difference within and between groups of Er:YAG laser and SRP.²⁷ This result might be because of short evaluation periods, which are not enough for reepithelialization and soft tissue healing (12 and 3 days post-treatment). IL-1β and MMP-8 results within groups in the present study are in accordance with our clinical results.

Moreover, the Er,Cr:YSGG laser was chosen in this clinical trial because it has been shown that erbium lasers have an affinity to water and hydroxyapatite, which make them both soft and hard tissue lasers. The reasons why results are in favor of the test group could be that laser treatment significantly increases epithelial cell proliferation and migration and that laser treatment also enhances the adhesion and proliferation of gingival fibroblasts on root surfaces.^6,29,48 These results can also be due to biomodification of the root surface texture and smear layer removal by the Er,Cr:YSGG laser.²⁹

Since the clinical studies directly comparing the use of the Er,Cr:YSGG laser^15,39,49,50 with conventional root planing are not sufficient, we mostly made comparisons with Er:YAG laser studies.^{23

–28,36,46} Differences in laser parameters, treatment groups, application of nonsurgical periodontal therapy, evaluation periods, and inclusion criteria such as smoking and laser type may explain the main reason for the discrepancies between the study results. Therefore, our comparisons with other clinical studies were restricted.

Since smoking has a negative impact on periodontal therapy, we did not include either smokers or former smokers in the study.^51,52

The aim of the full-mouth approach in this study is to prevent bacterial transport from untreated sites to treated sites.

Further long-term studies evaluating results of the Er,Cr:YSGG laser in nonsurgical periodontal treatment as an alternative to root planing with hand instruments are needed. In addition, the present study could have been planned with an extra group that could have received treatment only with ultrasonic scalers.

Conclusions

Our results indicated that in addition to ultrasonic instrumentation, the use of the Er,Cr:YSGG laser has shown better clinical results than using Gracey curettes—a conventional method—in terms of pocket depth reduction and gingival bleeding, especially in deeper pockets.

Summary

Nonsurgical therapy of advanced chronic periodontitis using the ultrasonic scaler and Er,Cr:YSGG laser resulted in significantly greater improvements in clinical indices such as PD and BOP than conventional scaling and root planing.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

This study was financed by the Scientific Research Projects Coordination Unit of Istanbul University, project no. 20486.

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