Print this page Email this page Users Online: 224
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2013  |  Volume : 7  |  Issue : 2  |  Page : 59-65

Effect of low power diode laser 810 nm on TGF-β1 level in GCF in aggressive periodontitis


1 Department of Dental Laser Applications, National Institute of Laser Enhanced Sciences, Cairo University, Cairo, Egypt
2 Lecturer of Periodontology, Faculty of Oral and Dental Medicine, Cairo University, Cairo, Egypt
3 Lecturer of Clinical Pathology, Faculty of Medicine, Cairo University, Cairo, Egypt
4 Bachelor of Dental Surgery, October 6th University, Cairo, Egypt

Date of Web Publication3-Jan-2014

Correspondence Address:
Ramiz Radwan
Master Student, Medical Laser Applications, National Institute of Laser Enhanced Sciences, Cairo University, Giza
Egypt
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0976-2868.124266

Rights and Permissions
  Abstract 

Objective: To evaluate the effect of low power diode laser (LPDL) 810 nm as an adjunct to nonsurgical treatment of mild to moderate aggressive periodontitis (AgP). Background: AgP is a rapidly progressive severe form of periodontitis; conventional treatment depends on the concept of plaque control and bacterial eradication. Scaling and root planning (SRP) is the basic periodontal treatment, has its limitations, so new treatment modalities are needed. Materials and Methods: The use of low power laser was suggested as an adjunct to periodontal treatment, as it was proven earlier to have a positive biomodulatory effect on biological tissues if suitable parameters were used for the condition in hand. A split-mouth design clinical trial was performed. The laser group received both SRP plus laser, and the control group only received SRP. The clinical evaluation included periodontal pocket depth (PPD), clinical attachment loss (CAL), plaque index (PI), modified gingival index (MGI), and gingival recession (GR), were taken at baseline and at 3 months. Transforming growth factor beta 1 (TGF-β1) was screened by sampling gingival crevicular fluid (GCF) at baseline and at 1, 2, 3, and 4 weeks after treatment. Results: Showed a significant decrease of PPD and CAL in favor of laser group. PI, MGI, and GR showed no significant difference between both groups. TGF-β1 mean percentage showed a significant steady decrease in the laser group. Conclusion: Low power laser parameters in this clinical trial can be used as an adjunct to SRP in treatment of mild to moderate AgP.

Keywords: Aggressive periodontitis, biomodulation, diode laser, laser or low level laser therapy, transforming growth factor beta 1


How to cite this article:
Saafan A, El-Nahass H, Nasr AS, Radwan R. Effect of low power diode laser 810 nm on TGF-β1 level in GCF in aggressive periodontitis. J Dent Lasers 2013;7:59-65

How to cite this URL:
Saafan A, El-Nahass H, Nasr AS, Radwan R. Effect of low power diode laser 810 nm on TGF-β1 level in GCF in aggressive periodontitis. J Dent Lasers [serial online] 2013 [cited 2017 Mar 29];7:59-65. Available from: http://www.jdentlasers.org/text.asp?2013/7/2/59/124266


  Introduction Top


Periodontitis as specified by Page and Eke 2007 and Novak 2006 is an inflammatory disease caused by infection of the supporting tissues around the teeth, by forming a biofilm (plaque), and as a result destruction of the alveolar bone and periodontal ligament occur and in turn periodontal pockets and/or recessions are created. [1],[2]

Aggressive periodontitis (AgP) (Armitage 1999), [3] is a multifactorial, severe, rapidly progressive, and destructive form of periodontitis, characterized by rapid attachment loss, bone destruction in otherwise healthy individuals, the amount of bacterial plaque deposits are inconsistent with the severity of destruction (Noack and Hoffmann 2004). [4]

Standard approach for treating AgP as stated by Cobb 2002, and Research, Science, and Therapy Committee of the American Academy of Periodontology 2001 include scaling and root planning (SRP) in the early stages of disease with or without surgery in later phases, the surgical procedures mostly done with pocket depth greater than 5 mm. In case of no treatment the tooth will be lost as both the periodontal ligament and the surrounding alveolar bone are destroyed by the inflammatory process. [5],[6]

Aukhil 2000 reported about periodontal wound healing that it is a unique and complex process which requires the coordination between gingival connective tissue, periodontal ligaments, cementum, and alveolar bone. SRP most commonly results in repair by collagenous scar tissue. [7]

Green and Klink 1998 reported that platelets initiate tissue regeneration in case of trauma, during repair fibrin clot becomes full of platelets which release and degranulate two growth factors: Platelet derived growth factor (PDGF) and transforming growth factor beta (TGF-β). [8] Anila and Nandakumar 2006 indicated that growth factors released from platelets stimulate wound healing process. Periodontal wound healing involves gingival fibroblasts, gingival epithelial cells, periodontal ligament fibroblasts, and osteoblasts, all of which are important for tissue repair and hard tissue regeneration. [9]

Fiorellini et al., 2006 found that the gingival crevicular fluid (GCF) contains a lot of biochemical factors which can be used as a diagnostic or prognostic biomarker of the biological state of the periodontium in health and disease. [10] GCF serves as an indicator of periodontal disease and healing after therapy (Ebersole in 2003). [11] Reinhardt et al., 2010 recognized that GCF has a diagnostic value as describing the inflammatory events happening at a specific site, allowing for the periodic assessment during periodontal treatment or maintenance. [12]

Champagne et al., 2003 found that with periodontal diseases GCF is a convenient mean of collecting samples of inflammatory mediators and biomarkers, and that periodontitis is in relation with overall systemic inflammatory response of the individual and it is more patient based than site specific. [13]

Teles et al., 2010 indicated that periodontal diseases lead to the release of inflammatory mediators. Cytokine levels in AgP showed statistically significant difference in comparison to periodontally healthy subjects. [14]

According to Buduneli et al., 2001 TGF-β1 can be found in samples of GCF in both normal and inflamed gingival tissues. [15]

TGF-β superfamily, is subdivided into TGF-β1, TGF-β2, and TGF-β3, which regulates a variety of cellular processes such as wound healing, and also has an important regulatory role in the inflammatory process (Kingsley 1994, Hogan 1996, Massague 2000, Attisano and Wrana 2002, Chang et al., 2002, and Mohamed et al., 2007). [16],[17],[18],[19],[20],[21]

Ruskin et al., 2000 reported that TGF-β found in platelets, and can stimulate a variety of cells such as mesenchymal stem cells which when stimulated provide wound healing cells. In vitro, TGF-β promotes extracellular matrix production in periodontal ligament fibroblasts. [22]

A lot of methods were studied in order to improve the wound healing outcome, either biological such as stem cell therapy, platelet rich plasma, and gene therapy; or physical such as electrical stimulation, magnetic field, warming, hyperbaric oxygen, topical oxygen, and laser or low level laser therapy (LLLT) (Kaskos and Al-Hasan 2011). [23]

LLLT also known as biostimulation, photobiomodulation because it needs an optimal dose of light for any particular application, lower doses give diminished therapeutic outcome, high doses may give a negative outcome. Visible or near infrared light are the most commonly used wavelengths. LLLT remains controversial because of the incompletely understood biochemical mechanisms underlying its positive effects, and also the complexity of choosing suitable light parameters (Hamblin and Demidova 2006). [24]

Castro et al., 2006 have concluded that treating periodontal patients with a combination of SRP and laser is beneficial and provides better results than any of them as a sole treatment. [25]

Hakkinen et al., 2000 specified that fibroblasts play an important role in the process of tissue healing. [26] Kreisler et al., 2002 reported that using LLLT was recommended for fibroblasts biostimulation and healing process acceleration. [27]

LLLT influences periodontal ligaments fibroblasts and gingival fibroblasts positively, hence has a beneficial effect on periodontal wound healing (Basso et al., 2012, Schwarz et al., 2009, and Choi et al., 2010), [28],[29],[30] also induced expression of TGF-β1 in cultured human fetal osteoblast cell line (Pyo et al., 2012), [31] and increased production of TGF-β1 measured by an enzyme-linked immunosorbent assay (ELISA) in cultured human osteoblast-like cells (Khadra et al., 2005). [32]

Aim of the study

To evaluate clinically and immunologically the effect of low power diode laser (LPDL) 810 nm as an adjunct to nonsurgical periodontal treatment of mild to moderate AgP.


  Materials and Methods Top


A total of 32 periodontal defects in eight patients with untreated AgP [Figure 1] and [Figure 2], otherwise healthy individuals, with average pocket depth of ≤5 mm [Figure 3], were introduced in this split mouth clinical trial. All the participants gave their informed consent prior to participation and local institutional research board approval was taken. All patients with factors that may affect the final results were excluded. All patients had a healthy systemic condition according to modified Cornell medical index (Abramson 1966). [33]
Figure 1: Clinical photo of aggressive periodontitis

Click here to view
Figure 2: Panoramic X-ray film of AgP

Click here to view
Figure 3: Periodontal pocket depth at baseline with average pocket depth of ≤5 mm

Click here to view


On day 1, gentle removal of the dental plaque and isolation was done before collecting the first GCF sample, followed by four postoperative weekly samples, using three absorbing paper points; size 40 [Figure 4], for 30 sec. each, separately in three consecutive placements, samples with signs of saliva or blood were discarded. Then each sample was preserved inside an eppendorf (size 1.5) filled with 200 μl of phosphate buffered saline, and finally centrifuged for 10 min on a speed of 1,500 rpm, before being freezed (−40΀C) till they were tested with the ELISA kits (KOMABIOTECH biotechnology, Seoul, Korea) for detection of TGF-β1 level change in GCF.
Figure 4: Sample collection of gingival crevicular fluid with absorbing paper point size 40

Click here to view


On day 1, oral hygiene measures were instructed, SRP was performed and periodontal pocket depth (PPD), clinical attachment loss (CAL), modified gingival index (MGI), plaque index (PI), and gingival recession (GR) were recorded. After 3 months, patients came back for reevaluation and postoperative measurements recording.

Laser irradiation schedule with a total of eight sessions postoperatively; started with immediate postoperative session, and then the following sessions were delivered on a "day on day off" basis within 17 days. LPDL device locally manufactured (Photon Scientific, Industrial Area, Qaliub, Egypt) was used [Figure 5], which was CW 810 nm with power output of 200 mW (at the end of the intraoral tip in contact mode) [Figure 6], energy of 16 J, and the total exposure time was 80 sec. per defect. The spot size was 4 mm circle so; the power density was 0.2 W/cm 2 , and the energy density was 16 J/cm 2 .
Figure 5: Laser device used

Click here to view
Figure 6: Laser probe with intraoral tip

Click here to view


Statistical analysis was performed with IBM; (IBM Corporation],[ NY],[ USA.) Statistical Package for Social Sciences (SPSS); (SPSS, Inc., an IBM Company) statistics version 20 for windows, and the significance level was set at P ≤ 0.05.


  Results Top


Laser group showed statistically significantly higher mean % reduction in PPD than control group (P = 0.035). Laser group showed statistically significantly higher mean % reduction in CAL than control group (P = 0.044). GR showed no statistically significant difference between the two groups (P = 0.317). PI showed no statistically significant difference between the two groups (P = 0.956). MGI showed no statistically significant difference between the two groups (P = 0.752).

After 1 week, laser group showed statistically significantly lower mean % increase in TGF-β1 results than control group (P = 0.002). After 2 weeks, there was no statistically significant difference between the two groups (P = 0.819). After 3 weeks, laser group showed statistically significantly lower mean % decrease in TGF-β1 results than control group (P = 0.004). After 4 weeks, laser group showed statistically significantly lower mean % decrease in TGF-β1 results than control group (P < 0.001).


  Discussion Top


Most patients with periodontitis respond positively to SRP, apart from patients with AgP (Klokkevold et al., 2006). [34] Thus, the search continues for adjunctive therapeutic techniques in order to improve the healing outcome.

LPDL was used because of its biostimulatory effects including proliferation of several types of cells (fibroblasts and endothelial cells), collagen synthesis, release of growth factors, and cytokines (Dube et al., 2003, Stadler et al., 2000, Kreisler et al., 2003, and Enwemeka 2004). [35],[36],[37],[38] Furthermore, its ability to enhance wound healing, improve epithelialization (Ozcelik et al., 2008), [39] and promote healing (Guzzardella et al., 2003). [40]

ELISA assay was used as it was used before to confirm the role of TGF-β1 in periodontal wound healing and periodontal tissue regeneration (Elbarbary 2008), [41] reflecting the early inflammatory stage of periodontal wound healing in terms of enhanced permeability of gingival blood vessels and increased fluid passage through the vasculature into the extravascular space (Egelberg 1966). [42]

The device used was a diode 810 nm, the wavelength in the near-infrared range (diode lasers GaAlAs 780-890 nm) can penetrate several millimetres, thus used to stimulate deep cellular function, this justified the use of the special intraoral tip in contact mode on both sides of the defect (buccal and lingual) in order for the laser beam to be able to penetrate as deep as possible. Based on the Arndt Schultz law (small doses stimulate, medium doses inhibit, and large doses destroy) (Parker 2007), [43] energy density used was 16 J/cm 2 (Blaya et al.,) [44]

Laser group showed statistically significantly higher mean percentage of reduction in PPD and CAL than control group. This may be attributed to the effect of laser irradiation which enhance connective tissue attachment and promote wound healing by positively affecting the cells responsible for this process such as fibroblasts, endothelial cells, in addition to increased collagen synthesis. Kreisler et al., 2005 found similar results using 809 nm laser at power output of 1.0 W using a 0.6 mm optical fiber as an adjunct to SRP, in laser group a significantly higher reduction in PPD, and CAL were found between baseline and after 3 months. [45]

There was no statistically significant difference between the mean percentages of GR in the two groups, although at baseline GR of the laser group showed statistically significantly higher mean gingival recession than the control group. This could be due to the effect of laser application as it hindered further destruction of the attachment apparatus of the irradiated sites, thus helping in repair or regenerative process of the peridontium. In contrast Lai et al., 2009 used HeNe laser (output power of 0.2 mW for 10 min for a total of eight times in the first 3 months) with SRP in treatment of moderate to advanced chronic periodontitis (ChP) (PPD ≥5 mm), there was an increase in GR in both groups, plus there was no statistically significant differences in any clinical parameters between laser and control groups, [46] this could be due to the very long duration during which the total number of laser sessions were delivered, and the severity of the disease may implicate considering different treatment modalities.

PI showed no statistically significant difference when comparing the percentage of reduction between the two groups; this could be a result of using a split-mouth design for our study along with good oral hygiene measures that the patients followed meticulously. Our results were in contrast with a study conducted on patients with mild ChP by Pejcic et al., 2010, in which after SRP for both groups, laser group was subjected to 10 sessions of LLLT (670 nm), at the end there was a decrease in PI, GI, and bleeding on probing index (BOP) in both groups, it was concluded that LLLT together with SRP, gave better and longer-lasting results up to 6 months. [47]

By comparing the percentage of reduction of the two groups MGI showed no statistically significant difference between the two groups. In our study the inflammation in both groups was not considerably profound from the start, which could explain the reason of lack of difference between the two groups. On the contrary, Ribeiro et al., 2008 evaluated the auxiliary effect of the LLLT (660 nm, 35 mW, 8.8 J/cm 2 , for 10 s per site) with SRP, a total of three irradiation sessions started immediately postoperative plus two sessions in the following consecutive 2 days were applied. The results came with a reduction in GI of both laser and control groups, but without any statistically significant difference between them after 3 days. [48] Although this goes in accordance with the current study, there were some differences, as applying only three irradiation sessions, plus postoperative reevaluation was only performed after 3 days which is considered to be a very short follow-up period.

By comparing the percentage of change in TGF-β1 level of both groups it was found that, after 1 week laser group showed statistically significantly lower mean of percentage increase in TGF-β1 level than control group, after 2 weeks there was no statistically significant difference between the two groups, after 3 weeks laser group showed statistically significantly lower mean of percentage decrease in TGF-β1 level than control group, after 4 weeks laser group showed statistically significantly lower mean of percentage decrease in TGF-β1 level than control group, this indicated the constant decrease in inflammation in both groups with a more steady decrease in inflammation in the laser group than the control group (in comparison to baseline) along the period of the study, except for week 1 in both groups and week 3 in the control group where a peak of increase in the TGF-β1 percentage was evident which could refer to a possible attempt of tissue repair [Figure 7], this could be explained in the study made by Steinsvoll et al., 1999 in which they clarified that during periodontal disease TGF-β1 can alternate between pro-inflammatory and anti-inflammatory roles related to the nature of host response, and TGF-β1 levels have been shown to be higher in gingival tissues and GCF at sites of inflammation compared to healthy sites. [49] In contrast Aykol et al., 2011 evaluated the effect of LLLT (808 nm, 0.25 W, and 4 J/cm 2 on 1 st , 2 nd , and 7 th day) as an adjunct to SRP for smoking and nonsmoking patients with moderate to advanced ChP, results showed that TGF-β1 levels reduced statistically significantly between baseline and all time points (1, 3, and 6 months) for both groups after elimination of inflammation, and TGF-β1 level change in GCF did not show any significant difference between the LLLT and control groups, [50] this could be attributed to the extended periods between the GCF samples collection time points, which allowed for a longer period of healing, especially that TGF-β1 level increase mainly in the first 2 weeks postoperatively according to Kuru et al., 2004. [51]
Figure 7: Line chart representing mean % changes in transforming growth factor beta 1 results of the two groups (in comparison with baseline represented by the zero line)

Click here to view



  Conclusions and Summary Top


Within the circumstances of the study in hand and based on its results, it can be concluded that low power laser if used with the same parameters presented in this clinical trial can be of a benefit as an adjunctive treatment to conventional nonsurgical periodontal treatment of mild to moderate AgP.

 
  References Top

1.Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol 2007;78 Suppl 7:1387-99.  Back to cited text no. 1
    
2.Novak M. Classification of diseases and conditions affecting the periodontium. In: Newman M, Takei H, Klokkevold P, Carranza F, editors. Carranza′s Clinical Periodontology. 10 th ed. Phildelphia: Saunders Elsevier; 2006. p. 100-9.  Back to cited text no. 2
    
3.Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6.  Back to cited text no. 3
    
4.Noack B, Hoffmann T. Aggressive periodontitis. Periodontol 2004;1:335-44.  Back to cited text no. 4
    
5.Cobb CM. Clinical significance of non-surgical periodontal therapy: An evidence-based perspective of scaling and root planing. J Clin Periodontol 2002;29 Suppl 2:6-16.  Back to cited text no. 5
    
6.Research, Science and Therapy Committee of the American Academy of Periodontology. Treatment of plaque-induced gingivitis, chronic periodontitis, and other clinical conditions. J Periodontol 2001;72:1790-800.  Back to cited text no. 6
    
7.Aukhil I. Biology of wound healing. Periodontol 2000 2000;22:44-50.  Back to cited text no. 7
    
8.Green DM, Klink B. Platelet gel as an intraoperatively procured platelet-based alternative to fibrin glue. Plast Reconstr Surg 1998;101:1161-2.  Back to cited text no. 8
    
9.Anila S, Nandakumar K. Applications of platelet rich plasma for regenerative therapy in periodontics. Trends Biomater Artif Organs 2006;20:78-83.  Back to cited text no. 9
    
10.Fiorellini J, Kim D, Ishikawa S. The gingiva. In: Newman M, Takei H, Klokkevold P, Carranza F, editors. Carranza′s Clinical Periodontology. 10 th ed. Philadelphia: Saunders Elsevier; 2006. p. 46-67.  Back to cited text no. 10
    
11.Ebersole JL. Humoral immune responses in gingival crevicular fluid: Local and systemic implications. Periodontol 2000 2003;31:135-66.  Back to cited text no. 11
    
12.Reinhardt RA, Stoner JA, Golub JA, Lee HM, Nummikoski PV, Sorsa T, et al. Association of gingival crevicular fluid biomarkers during periodontal maintenance with subsequent progressive periodontitis. J Periodontol 2010;81:251-9.  Back to cited text no. 12
    
13.Champagne CM, Buchanan W, Reddy MS, Preisser JS, Beck JD, Offenbacher S. Potential for gingival crevice fluid measures as predictors of risk for periodontal diseases. Periodontol 2000 2003;31:167-80.  Back to cited text no. 13
    
14.Teles RP, Gursky LC, Faveri M, Rosa EA, Teles FR, Feres M, et al. Relationships between subgingival microbiota and GCF biomarkers in generalized aggressive periodontitis. J Clin Periodontol 2010;37:313-23.  Back to cited text no. 14
    
15.Buduneli N, Kütükçüler N, Aksu G, Atilla G. Evaluation of transforming growth factor-beta 1 level in crevicular fluid of cyclosporin A-treated patients. J Periodontol 2001;72:526-31.  Back to cited text no. 15
    
16.Kingsley DM. The TGF-beta superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes Dev 1994;8:133-46.  Back to cited text no. 16
    
17.Hogan BL. Bone morphogenetic proteins in development. Curr Opin Genet Dev 1996;6:432-8.  Back to cited text no. 17
    
18.Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol 2000;1:169-78.  Back to cited text no. 18
    
19.Attisano L, Wrana JL. Signal transduction by the TGF-beta superfamily. Science 2002;296:1646-7.  Back to cited text no. 19
    
20.Chang H, Brown CW, Matzuk MM. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev 2002;23:787-823.  Back to cited text no. 20
    
21.Mohamed A, Zaki S, Abbass H. Study of transforming growth factor-beta-1 in elderly with recent cerebrovascular stroke. Alex J Med 2007;43. Available from: http://www.med.alexu.edu.eg/journal/index.php/bulletin/article/view/95/90 [Last accessed on 2013 Dec 04].  Back to cited text no. 21
    
22.Ruskin JD, Hardwick R, Buser D, Dahlin C, Schenk RK. Alveolar ridge repair in a canine model using rhTGF-beta 1 with barrier membranes. Clin Oral Implants Res 2000;11:107-15.  Back to cited text no. 22
    
23.Kaskos H, Al-Hasan A. Effect of low level laser therapy on intra oral wound healing. Al-Rafidain Dent J 2011;11:105-12.  Back to cited text no. 23
    
24.Hamblin M, Demidova T. Mechanisms of low level light therapy. Proceedings SPIE 2006;6140:1-12.  Back to cited text no. 24
    
25.Castro GL, Gallas M, Nunez IR, Borrajo JL, Varela LG. Histological evaluation of the use of diode laser as an adjunct to traditional periodontal treatment. Photomed Laser Surg 2006;24:64-8.  Back to cited text no. 25
    
26.Hakkinen L, Uitto VJ, Larjava H. Cell biology of gingival wound healing. Periodontol 2000 2000;24:127-52.  Back to cited text no. 26
    
27.Kreisler M, Christoffers AB, Al-Haj H, Willershausen B, d′Hoedt B. Low level 809-nm diode laser-induced in vitro stimulation of the proliferation of human gingival fibroblasts. Lasers Surg Med 2002;30:365-9.  Back to cited text no. 27
    
28.Basso FG, Pansani TN, Turrioni AP, Bagnato VS, Hebling J, de Souza Costa CA. In vitro wound healing improvement by low-level laser therapy application in cultured gingival fibroblasts. Int J Dent 2012;2012:719452.  Back to cited text no. 28
    
29.Schwarz F, Aoki A, Sculean A, Becker J. The impact of laser application on periodontal and peri-implant wound healing. Periodontol 2000 2009;51:79-108.  Back to cited text no. 29
    
30.Choi EJ, Yim JY, Koo KT, Seol YJ, Lee YM, Ku Y, et al. Biological effects of a semiconductor diode laser on human periodontal ligament fibroblasts. J Periodontal Implant Sci 2010;40:105-10.  Back to cited text no. 30
    
31.Pyo SJ, Song WW, Kim IR, Park BS, Kim CH, Shin SH, et al. Low-level laser therapy induces the expressions of BMP-2, osteocalcin, and TGF-β1 in hypoxic-cultured human osteoblasts. Lasers Med Sci 2012;28:543-50.  Back to cited text no. 31
    
32.Khadra M, Lyngstadaas SP, Haanaes HR, Mustafa K. Effect of laser therapy on attachment, proliferation and differentiation of human osteoblast-like cells cultured on titanium implant material. Biomaterials 2005;26:3503-9.  Back to cited text no. 32
    
33.Abramson JH. The cornell medical index as an epidemiological tool. Am J Public Health Nations Health 1966;56:287-98.  Back to cited text no. 33
    
34.Klokkevold P, Nagy R. Treatment of aggressive and atypical form of periodontitis. In: Newman M, Takei H, Klokkevold P, Carranza F, editors. Carranza′s Clinical Periodontology. 10 th ed. Philadelphia: Saunders Elsevier; 2006. p. 693-705.  Back to cited text no. 34
    
35.Dube A, Bansal H, Gupta PK. Modulation of macrophage structure and function by low level He-Ne laser irradiation. Photochem Photobiol Sci 2003;2:851-5.  Back to cited text no. 35
    
36.Stadler I, Evans R, Kolb B, Naim J, Narayan V, Buehner N, et al. In vitro effects of low-level laser irradiation at 660 nm on peripheral blood lymphocytes. Lasers Surg Med 2000;27:255-61.  Back to cited text no. 36
    
37.Kreisler M, Christoffers AB, Willershausen B, d′Hoedt B. Effect of low-level GaAlAs laser irradiation on the proliferation rate of human periodontal ligament fibroblasts: An in vitro study. J Clin Periodontol 2003;30:353-8.  Back to cited text no. 37
    
38.Enwemeka CS, Parker JC, Dowdy DS, Harkness ES, Sanford LE, Woodruff LD. The efficacy of low-power lasers in tissue repair and pain control: A meta-analysis study. Photomed Laser Surg 2004;22:323-9.  Back to cited text no. 38
    
39.Ozcelik O, Cenk Haytac M, Kunin A, Seydaoglu G. Improved wound healing by low-level laser irradiation after gingivectomy operations: A controlled pilot study. J Clin Periodontol 2008;35:250-4.  Back to cited text no. 39
    
40.Guzzardella GA, Torricelli P, Nicoli-Aldini N, Giardino R. Osseointegration of endosseous ceramic implants after postoperative low-power laser stimulation: An in vivo comparative study. Clin Oral Implants Res 2003;14:226-32.  Back to cited text no. 40
    
41.Elbarbary A. Assessment of transforming growth factor beta1 level in gingival crevicular fluid after periodontal surgery. Thesis of master degree of oral medicine and periodontology, Cairo University, Faculty of Oral and Dental Medicine, Department of Periodontology; 2008. p. 34-48.  Back to cited text no. 41
    
42.Egelberg J. Permeability of the dentogingival blood vessels. 1. Application of the vascular labeling method and gingival fluid measurements. J Periodontal Res 1966;1:180-91.  Back to cited text no. 42
    
43.Parker S. Low-level laser use in dentistry. Br Dent J 2007;202:131-8.  Back to cited text no. 43
    
44.Blaya DS, Guimarães MB, Pozza DH, Weber JB, de Oliveira MG. Histologic study of the effect of laser therapy on bone repair. J Contemp Dent Pract 2008;9:41-8.  Back to cited text no. 44
    
45.Kreisler M, Al Haj H, d′Hoedt B. Clinical efficacy of semiconductor laser application as an adjunct to conventional scaling and root planing. Lasers Surg Med 2005;37:350-5.  Back to cited text no. 45
    
46.Lai SM, Zee KY, Lai MK, Corbet EF. Clinical and radiographic investigation of the adjunctive effects of a low-power He-Ne laser in the treatment of moderate to advanced periodontal disease: A pilot study. Photomed Laser Surg 2009;27:287-93.  Back to cited text no. 46
    
47.Pejcic A, Kojovic D, Kesic L, Obradovic R. The effects of low level laser irradiation on gingival inflammation. Photomed Laser Surg 2010;28:69-74.  Back to cited text no. 47
    
48.Ribeiro IW, Sbrana MC, Esper LA, Almeida AL. Evaluation of the effect of the GaAlAs laser on subgingival scaling and root planning. Photomed Laser Surg 2008;26:387-91.  Back to cited text no. 48
    
49.Steinsvoll S, Halstensen TS, Schenck K. Extensive expression of TGF-beta1 in chronically-inflamed periodontal tissue. J Clin Periodontol 1999;26:366-73.  Back to cited text no. 49
    
50.Aykol G, Baser U, Maden I, Kazak Z, Onan U, Tanrikulu-Kucuk S, et al. The effect of low-level laser therapy as an adjunct to non-surgical periodontal treatment. J Periodontol 2011;82:481-8.  Back to cited text no. 50
    
51.Kuru L, Griffiths GS, Petrie A, Olsen I. Changes in transforming growth factor-beta1 in gingival crevicular fluid following periodontal surgery. J Clin Periodontol 2004;31:527-33.  Back to cited text no. 51
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusions and ...
References
Article Figures

 Article Access Statistics
    Viewed2039    
    Printed52    
    Emailed1    
    PDF Downloaded297    
    Comments [Add]    

Recommend this journal