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Photomedicine and Laser Surgery

Volume XX, Number XX, 2016 Original Research


ª Mary Ann Liebert, Inc.
Pp. 1–5
DOI: 10.1089/pho.2016.4117

Role of Low-Level Laser Therapy as an Adjunct


to Initial Periodontal Treatment in Type 2 Diabetic Patients:
A Split-Mouth, Randomized, Controlled Clinical Trial

Oya Demirturk-Gocgun, DDS, PhD,1 Ulku Baser, DDS, PhD,1 Gokce Aykol-Sahin, DDS, PhD,2
Nevin Dinccag, MD, PhD,3 Halim Issever, MD, PhD,4 and Funda Yalcin, DDS, PhD1

Abstract

Objective: In this split-mouth clinical trial, we evaluated the clinical benefits of low-level laser therapy (LLLT)
as an adjunct to nonsurgical periodontal treatment in patients with type 2 diabetes mellitus (DM). Background
data: The impaired wound healing seen in diabetic patients may affect the results of periodontal treatment and
may require an additional approach. Materials and methods: In total, 22 chronic periodontitis patients with type
2 DM were included. Applying a split-mouth design, two quadrants were treated with only scaling and root
planing (SRP) as the control and those in the other two were treated with SRP + LLLT as the test sites in each
patient. An 808 nm GaAlAs diode laser was performed in the test sites at the energy density of 4.46 J/cm2 on days
1, 2, and 7 after SRP. Plaque index (PI), probing depth (PD), bleeding on probing (BOP), and clinical attachment
level were measured at baseline and again at 1 and 3 months after treatment. Deep periodontal pockets (PD
‡4 mm) were evaluated separately. Results: Test sites showed significant improvement in PI and BOP in deep
pockets at the 1-month follow-up period ( p < 0.001 and <0.001, respectively), whereas no difference was found
between the control and the test sites in other periodontal parameters. Conclusions: LLLT during periodontal
treatment offered minimal short-term additional benefit in deep pocket healing in patients with type 2 DM.

Keywords: diabetes mellitus type 2, laser therapy, low level, periodontology

Introduction LLLT as an adjunct to nonsurgical periodontal treatment in


periodontal wound healing in smokers and nonsmokers with
D iabetes Mellitus (DM) is caused by a deficiency in
insulin or its action, resulting in hyperglycemia and
hyperlipidemia, which are involved in the development of
chronic periodontitis were evaluated and that previous study
indicated that LLLT, as an adjunctive therapy to nonsurgical
periodontal treatment, improved periodontal healing.12 In
many systemic and oral complications, such as period-
the current study, because DM, like smoking, affects the
ontitis.1,2 Studies have shown that type 2 DM is a risk factor
healing of periodontal tissues, it was hypothesized that LLLT
for periodontal diseases and those patients with diabetes
would have positive effects on the microcirculation and on
show higher prevalence and severity of periodontitis com-
collagen and cytokine production, which are negatively af-
pared with nondiabetic patients.3–5 The impaired wound
fected by DM. Thus, the purpose of this split-mouth, ran-
healing seen in diabetic patients may affect the results of
domized, controlled clinical trial was to evaluate the effects
periodontal treatment and may require an additional ap-
of LLLT as an adjunct to nonsurgical periodontal treatment
proach. According to the evidence, low-level laser therapy
on clinical parameters in type 2 DM patients with chronic
(LLLT), also called photobiomodulation, has potential utility
periodontitis.
in accelerating the inflammatory response of wound healing.
Clinical studies have shown that LLLT promotes wound
Materials and Methods
healing by accelerating inflammation,6 collagen synthesis,7
healing time, and strength acquisition.8 Further, the studies The study was approved by the Research Ethics Com-
about LLLT as a treatment method for diabetic ulcers have mittee of Istanbul University of Medical Sciences (protocol
shown positive results.9–11 In a previous study, the effects of number: 2012/1467/1223). Written informed consent was
1
Department of Periodontology, Faculty of Dentistry, Istanbul University, Istanbul, Turkey.
2
Department of Periodontology, Faculty of Dentistry, Okan University, Istanbul, Turkey.
3
Division of Diabetes, Department of Internal Medicine, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey.
4
Department of Biostatistics, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey.

1
2 DEMIRTURK-GOCGUN ET AL.

obtained from all patients before their enrollment in the Table 1. Parameters of LLLT
study. The study protocol was approved and registered un- Energy per point/per tooth 1.25/5 J
der International Clinical Trials Registry Platform with the Power density 0.89 W/cm2
Thai Clinical Trials Registry, TCTR20150730001. Energy density/per point 4.46 J/cm2
Between October 2013 and February 2014, 80 type 2 DM Duration of each point 5 sec
patients being followed as outpatients in the Department of Four points/per gingiva 20 sec
Endocrinology, Istanbul Medical Faculty, Istanbul Uni- of root surface
versity, were screened. Patients who had type 2 DM were Frequency of the treatment 3 times (days 1, 2, and 7)
selected and classified based on the criteria of the American Cumulative dose for 3 days 13.38 J/cm2
Diabetic Association (2011) and glycated hemoglobin levels LLLT, low-level laser therapy.
(HbA1C).13 All diabetic patients were followed up regularly
in the department of endocrinology and all had stable dia-
betes. Among the type 2 DM patients, 22 patients with
reference point. A trained dentist, who was blinded to the
moderate to severe chronic periodontitis were selected for
treatment received by the patients, conducted periodontal
the study,14 and periodontal disease severity was defined
examinations.
according to Page and Eke.15
Exclusion criteria were any kind of periodontal treatment
during the last 6 months or use of antibiotics during the last 3 Statistical analysis
months, smoking, acute oral or systemic infection, periodontal
abscess, hemorrhagic disorders, autoimmune diseases, preg- For sample size calculation, BOP% was used as the pri-
nancy, or <15 teeth and partial dentures. Teeth with fixed mary outcome variable. According to the results of the
prosthodontics, and a mobility grade of III or pockets deeper power analysis, a sample size of 80 quadrants in 20 par-
than 10 mm in the studied areas were not evaluated. ticipants was identified for 80% statistical power, b = 0.20,
All patients received oral hygiene instructions and su- and a = 0.05 (to detect D = 10%).
pragingival scaling in two appointments, 1 week apart, be- The data collected were analyzed using a statistical soft-
fore root planing treatment. Full-mouth subgingival scaling ware package (SPSS, version 15.0; SPSS, Chicago, IL). Sites
and root planing (SRP) under local anesthesia (Ultracain were divided into two subgroups according to initial PD23:
DS; Aventis Pharmacheuticals, Istanbul, Turkey) was per- shallow pockets (0–3 mm); moderate and deep pockets
formed by the same operator in a single appointment for (4–10 mm). Differences between test and control sites and
each patient in all groups using hand instruments (Gracey between different time points were analyzed using the Mann–
Curets; Hu-Friedy, Chicago, IL) and ultrasonic devices Whitney U test and Wilcoxon signed-rank test, respectively.
(Cavitron; Dentsply, York, PA). Statistical significance was set at the 99% confidence level
The study was performed according to a split-mouth de- ( p < 0.01) for the Mann–Whitney U test and 95% ( p < 0.05)
sign, and each patient was included in a clinical protocol for the Wilcoxon signed-rank test.
consisting of two different modalities: teeth were treated by
SRP alone (control site) and by SRP followed by LLLT (test Results
site). Two quadrants were randomly assigned to the control
and two to the test group for each patient. Randomization Descriptive results
was performed using a computer-generated random alloca- Twenty-two participants attended the baseline examina-
tion table. Each selected segment first received a code tion, treatment, and the follow-up appointments over a 3-
number, and one of the study coordinators used a computer- month period. The total numbers of test and control sites
generated table to randomly allocate each quadrant to the were 1518 and 1548, and the test and control sites with PD
SRP (control, n = 22) or SRP + LLLT (test, n = 22) group. ‡4 mm were 698 and 669, respectively. Demographic vari-
A GaAlAs diode laser (k = 808 nm, Fotona XD-2; FOTONA ables described in Table 2.
D.O.O., Ljubljana, Slovenia) was used in this study. The
laser (output power, 0.25 W; continuous mode; handpiece,
R24-B; spot diameter, 6 mm; spot size, 0.28 cm2) was applied Table 2. Descriptive Parameters of the Study Group
with noncontact technique to the root surfaces through the
No. of patients 22
labial and oral gingiva at the test sites after the periodontal Mean age (min/max years) 41/72, 50.50 – 8.72
treatment. The parameters16–20 applied in the protocol are (mean – SD)
described in Table 1. Female (n, %) 15, 68.2
Clinical periodontal parameters were bleeding on probing Male (n, %) 7, 31.8
(BOP), plaque index (PI),21 gingival index (GI),22 probing Pocket depth ‡4 mm (%) 44.5, 22.7 (test)/21.8 (control)
depth (PD), and clinical attachment level (CAL). The pri- Diabetes duration (min/ 3/13, 5.40 – 2.55
mary outcome was BOP changes in deep pockets of the test max years) (mean – SD)
and control sites over the 3-month follow-up period. PI, GI, HbAIc at baseline (%) 5.50/10.90, 7.45 – 1.43
PD, and CAL were our secondary outcomes. All measure- (min/max) (mean – SD)
ments were recorded at six sites per tooth (mesio-, mid-, and Oral antidiabetic 15, 68.2
therapy (n, %)
disto-vestibular, and mesio-, mid-, and disto-palatal) at base- Oral antidiabetic + insulin 7, 31.8
line and at 1 and 3 months after treatment with a periodontal therapy (n, %)
Williams probe (PW6; Hu-Fredy, Chicago, IL), calibrated in
millimeters. The cemento–enamel junction was used as a SD, standard deviation.
LLLT ON DIABETIC PATIENTS 3

Table 3. Differences in Clinical Parameters


Parameter Difference Difference
mean – SD Baseline 1 Month (0- to 1-month) p* 3 Months (0- to 3-month) p{
PI
Test 1.81 – 0.36 0.91 – 0.39 0.89 – 0.38 0.000 0.74 – 0.26 1.06 – 0.31 0.000
Control 1.78 – 0.36 1.06 – 0.32 0.71 – 0.34 0.000 0.81 – 0.20 0.97 – 0.34 0.000
p* 0.122 0.364
BOP (mm)
Test 0.88 – 0.11 0.39 – 0.17 0.49 – 0.15 0.000 0.33 – 0.15 0.54 – 0.17 0.000
Control 0.87 – 0.14 0.44 – 0.16 0.43 – 0.16 0.000 0.33 – 0.16 0.54 – 0.19 0.000
p* 0.225 0.954
PD (mm)
Test 3.94 – 0.68 2.80 – 0.58 1.13 – 0.31 0.000 2.74 – 0.54 1.20 – 0.53 0.000
Control 3.86 – 0.57 2.79 – 0.56 1.06 – 0.23 0.000 2.69 – 0.46 1.16 – 0.30 0.000
p* 0.395 0.769
CAL (mm)
Test 4.30 – 1.01 3.10 – 0.89 1.20 – 0.34 0.000 3.14 – 0.98 1.16 – 0.89 0.000
Control 3.91 – 1.06 2.99 – 0.73 0.92 – 0.75 0.000 2.89 – 0.62 1.02 – 0.78 0.000
p* 0.123 0.573
*Mann–Whitney U test, p < 0.01.
{
Wilcoxon test, p < 0.05.
BOP, bleeding on probing; CAL, clinical attachment level; PD, probing depth; PI, plaque index.

Clinical parameters baseline and the first month. The reduction in PI was also
There was no statistically significant difference in the significantly greater in the test than in the control sites be-
clinical baseline measurements (PI, BOP, PD, and CAL) tween baseline and the third month. There was no significant
between the test and control sites (Table 3). Within the sites, difference between control and test sites in PD or CAL
statistically significant improvements ( p < 0.05) were noted changes at follow-up.
for PI, BOP, PD, and CAL when baseline values were
compared with the 3-month follow-up evaluation (Table 3).
Discussion
The improvements in these clinical parameters were slightly
better in the test sites, but the differences were not statisti- LLLT has been shown to be an effective modality in
cally significant ( p > 0.01). patients who suffer from diabetic wounds, especially for
The clinical measurements of deep pockets were analyzed diabetic foot ulcers.10 Research findings to date, based on
and are shown in Table 4. BOP and PI scores showed sta- in vitro animal and human studies, have shown that LLLT
tistically significant improvements in the test sites between can play a useful role in healing chronic diabetic ulcers

Table 4. Differences in Clinical Parameters (>4 mm PD)


Parameter Difference Difference
mean – SD Baseline 1 Month (0- to 1-month) p* 3 Months (0- to 3-month) p{
PI
Test 1.98 – 0.60 1.02 – 0.86 0.95 – 0.93 0.000 0.87 – 0.80 1.11 – 0.88 0.000
Control 1.96 – 0.60 1.25 – 0.82 0.71 – 0.90 0.000 0.97 – 0.78 0.99 – 0.92 0.000
p* 0.000 0.000
BOP (mm)
Test 0.94 – 0.23 0.48 – 0.50 0.46 – 0.51 0.000 0.40 – 0.49 0.54 – 0.52 0.000
Control 0.93 – 0.26 0.59 – 0.49 0.33 – 0.52 0.000 0.40 – 0.49 0.52 – 0.54 0.000
p* 0.000 0.657
PD (mm)
Test 5.31 – 1.08 3.37 – 1.28 1.93 – 1.09 0.000 3.17 – 1.19 2.14 – 1.14 0.000
Control 5.30 – 0.96 3.41 – 1.23 1.88 – 1.14 0.000 3.24 – 1.15 2.05 – 1.11 0.000
p* 0.808 0.337
CAL (mm)
Test 5.73 – 1.45 3.90 – 1.65 1.94 – 1.13 0.000 3.60 – 1.51 2.13 – 1.19 0.000
Control 5.53 – 1.15 3.68 – 1.42 1.90 – 1.15 0.000 3.48 – 1.34 2.04 – 1.14 0.000
p* 0.854 0.255
*Mann-Whitney U test, p < 0.01.
{
Wilcoxon test, p < 0.05.
4 DEMIRTURK-GOCGUN ET AL.

resistant to conventional treatments.9,24 The use of LLLT in BOP reduction in the first month of the test sites was not
periodontal treatment is still controversial. One study has maintained to the third month. Thus, given these results,
shown no additional benefit,25 whereas others have shown there is a need to evaluate the effects of different dosages on
that LLLT has demonstrable clinical efficacy, including our periodontal tissues in diabetic patients. Further studies are
previous study that showed additional improvement in also required to establish optimal treatment protocols, such
smokers.12,26–29 The present study was conducted from the as wavelength, fluency, intensity, exposure time, and total
perspective that more dramatic changes may occur among duration of the treatment.
patients with impaired wound healing, such as those with
diabetes mellitus (DM). Conclusions
Limited clinical research was found in the literature
when the search was focused on adjunctive effects of LLLT This split-mouth, randomized clinical trial indicated that
during the periodontal therapy in patients with DM2.30,31 the use of a low-level laser as an adjunct to SRP showed a
Although there were methodological differences with our minor short-term additional benefit on gingival bleeding, but
study, two studies reported that the effects of LLLT on it did not significantly enhance other clinical parameters.
periodontal tissues were mediated by DM.30,31 A histolog-
ical study conducted by Obradović et al.30 reported that Acknowledgments
more pronounced signs of gingival tissue healing were ob-
served after applying LLLT (670 nm, 2 J/cm2) as an adjunct This work was supported by the Scientific Research
to nonsurgical periodontal treatment in patients with type Projects Coordination Unit of Istanbul University, project
1 and type 2 DM. A subsequent study evaluated the effects number; T-39791. The authors declare that there are no
of LLLT by exfoliative cytology in patients with DM conflicts of interest in this study. No external funding, apart
and gingival inflammation; more pronounced GI reduction from the support of the authors’ institutions, was available
and lower cellular parameters were noticed on the laser- for the study.
treated side of the jaw than on the nonlaser side.31
The present study was designed to evaluate the role of Author Disclosure Statement
LLLT as an adjunct to nonsurgical periodontal treatment in
deep pockets among patients with type 2 DM. When deep No competing financial interests exist.
pockets were compared, test sites showed significant im-
provements in BOP between baseline and 1 month. LLLT References
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