Background: Chronic periodontitis (CP) is a common medical problem associated with non-insulin dependent diabetes mellitus (NIDDM) that affects about 47% of adult worldwide. The conventional therapy of CP is scaling and root planning (SRP). Although SRP is the golden therapy for CP,  it cannot eliminate the whole bacteria within periodontal tissues. Therefore, the need for innovative adjunct therapy for effective management of CP.

Objective: Our study aimed to assess the value of LILT added to SRP upon periodontal inflammation in NIDDM Saudi patients with CP.

Material and methods: Forty six NIDDM Saudi patients with chronic periodontitis (25 men and 21 women), their age ranged from 31- 58 year (mean 41.2±5.17 year) participated in the study. The participants randomly divided between 2 equal groups. Group (A) received conventional treatment for CP that composed of scaling and root planing (SRP group); while Group (B) received low intensity laser therapy conventional treatment for CP (SRP+LILT group).

Results: Mean values of IL-6, TNF-α, HBA1c, Plaque index, Probing pocket depth and gingival index reduced significantly after treatment in both groups. However, comparison between both groups after treatment revealed significant differences between group (A) and group (B). Moreover, group (B) received SRP+LILT gained greater reduction in the measured parameters.

Conclusion: Low intensity laser therapy as an effective adjunct to periodontal therapy upon periodontal inflammation in NIDDM Saudi patients with CP.

Keywords: periodontal therapy, non-insulin dependent diabetes mellitus, chronic periodontitis, low intensity laser therapy

SRP, scaling and root planning; CP, chronic periodontitis; NIDDM, non-insulin dependent diabetes mellitus; LILT, low level laser therapy

Chronic periodontitis (CP) means inflammatory disorder that destroys the gingiva and is one of the most prevalent chronic dental infection of bacterial origin in adults affect about 90% of people and 22% of diabetic patients globally.¹ Chronic periodontitis destroy the teeth supporting structures that lead to progressive alveolar bone and soft tissue destruction associated with gingival recession and formation of deep pocket.²

Poor glucose control associated with non-insulin dependent diabetes mellitus (NIDDM) is an important risk factor for CP and systemic inflammation.^3,4 In the other hand CP which has a negative effect on glucose control.⁵ Moreover, systemic inflammatory associated with  CP  increased the risk of some disorders as renal failure, cardiovascular disorders and diabetes.⁶

Scaling and root planing (SRP) is a conventional therapy for CP associated with some limitations  in managing  deep periodontal pockets.⁷ Therefore, many pharmacological adjuncts include antibiotics, anti-inflammatory and anticytokines were used to control inflammation and reduce bacterial.^8‒12 In addition, low level laser therapy (LILT) considered as an adjuncts to conventional therapy for CP.¹³ However, LILT Laser has excellent tissue ablation ability with a strong bactericidal effect as laser treatment improve the ability to access areas that are impossible to reach with conventional mechanical treatment.^14‒16 While, the accurate LLLT anti-inflammatory control mechanism of  CP remains inconclusive. Therefore, this study aimed to assess the value of LILT added to SRP upon periodontal inflammation in NIDDM Saudi patients with CP.

Subjects

Forty six  NIDDM Saudi patients with chronic periodontitis  (25 men and 21 women), their age ranged from 31-58 year (mean 41.2±5.17 year) were selected from the Department of Periodontics, King Fahd Hospital at Jeddah. Inclusion criteria included NIDDM patients with ≥4 periodontal pockets and probing depth≥5mm. However, exclusion criteria included smoking, autoimmune disorders, pregnancy, hemorrhagic disorders, acute illness, intake of anticoagulant, antibiotics and corticosteroid therapy during the previous three months. The participants randomly divided between 2 equal groups. Group (A) received conventional treatment for CP that composed of scaling and root planing (SRP group); while Group (B)  received low intensity laser therapy conventional treatment for CP  (SRP+LILT group).

Measurements

Periodontal parameters: Degree of periodontal indices were assessed by gingival index (GI) that was  measured from 0 (indicated healthy gingiva) to 3 (indicated spontaneous bleeding, severe inflammation), the level of hygiene was assessed by plaque index (PI) that was  measured from 1 (indicated presence of plaque detectable with probe) to 3 (abundant accumulation of plaque) and the pocket depth (PD) that measure the distance between base of the pocket and  the free gingival margin, the values were converted into a score called T-score that was  measured from 0 (PD ranged from 0 to 2mm) to 3 (PD˃6mm).^17‒19 

Biochemical parameters: From all participant an overnight fasting venous brachial blood sample was drained in clean test tube has few ml of K2EDTA for detection of glycosylated hemoglobin (HBA1c) using the standard colorimetric method with automated HbA1c analyzer (Quo-Lab® HbA1c). In addition, ELISA kits were used for the measurement of tumor necrosis factor-alpha (TNF-α) and  interleukin-6 (IL-6)  levels in the gingival crevicular fluid samples (Diaclone SAS®, Besançon, Bourgogne- Franche- Comté, France).²⁰

Procedures

The participants randomly divided between 2 equal groups

Group (A) : Twenty three NIDDM patients CP received conventional treatment for CP  that composed of scaling and root planing (SRP group) to enhance periodontal tissue  healing that included scaling that consisted of removal of tartar and plaque from supragingival and subgingival tooth surfaces mucobacterial by using inserts fixed on an ultrasonic scaler. However, root planning that consisted of removing  granulation tissue, subgingival calculus deposits, infected & necrotic cementum,  in addition to abolishing root surface irregularities by using manual tools as curettes for 3 months.

Group (B): Twenty three NIDDM patients CP received conventional treatment for CP  that composed of scaling and root planing in addition to low intensity laser therapy (LILT) (SRP+LILT group)  using a 940 nm diode laser (ezlase™ soft tissue diode laser–Biolase Technology Inc.). Wave length was 940nm, application power was 3 W,  the optical diameter fiber and tips was 300-400μ,  pulse frequency was 15Hz, fluency was 1.2 J/mm², pulse duration and relaxation time equal 10 and 20 millisecond respectively for 3 months. 

Statistical analysis

Comparison between mean values of the investigated before and after the study in both groups was calculated with Paired –t- test. However, comparison between groups was calculated with independent –t- test (P<0.05).

Forty-six participants enrolled in group (A) received SRP (n=23; 13 males and 10 females), while group (B) received SRP + laser therapy (n=23; 12 males and 11females). No statistical significant difference has been found between both groups regarding the criteria of participants (Table 1).

Mean values of TNF-α, IL-6, HBA1c, Plaque index, Probing pocket depth and Gingival index reduced significantly after treatment in both groups (Table 2 & 3). However, comparison between both groups after treatment revealed significant differences between group (A) and group (B). Moreover, group (B) received SRP+ LILT gained greater reduction in the measured parameters (Table 4).

Periodontal diseases are 2.8 times more among diabetic patients with hyperglycemia about 5 times higher risk of oral infections than non-diabetic subjects.²¹ However, CP is the 6^th complication of diabetes.²² In the other hand, periodontal therapy improves metabolic control in diabetics.²³ Our study aimed  to assess the value of LILT added to SRP upon periodontal inflammation in NIDDM Saudi CP patients. The outcomes of our study proved that SRP added to LLLT significantly reduced the GCF levels of TNF-α  and IL-6  greater than  SRP alone  in NIDDM patients with CP, these findings agreed with many studies. Sun et al. stated that conventional treatment improved inflammatory cytokines in NIDDM patients with CP.²⁴ However, Kocak et al.²⁵ proved that adjunct LLLT to SRP significantly reduced GCF IL-6  with no significant change in GCF IL-8  among NIDDM patients with CP.²⁵ While, Calderin et al.²⁶ reported that 2 months of adjunct LLLT to SRP significantly reduced GCF TNF-α in patients with CP. Also, Gundogar et al.²⁷ and Üstün et al.²⁸ mentioned that adjunct LLLT to SRP significantly reduced GCF cytokines in patients with CP. Moreover, Lee et al.²⁹ mentioned that LLLT significantly reduced the pro-inflammatory genes expression in periodontal inflammatory disease.²⁹ In the other hand, Kellesarian  et al.³⁰ conducted a systematic review on 22 randomized control trials and reported that the impact of adjunct LLLT to SRP upon pro-inflammatory cytokines expression in CP patients was inconclusive.

Concerning the periodontal parameters, the study results showed a significantly  reduced Plaque index, Probing pocket depth  and Gingival index  that indicated improvement in periodontal wound healing after  3 months of SRP adjuvant LLLT which agreed with Ustun et al.³¹  reported that 810 nm diode laser can cause significant reduction in GCF and IL-1β compared to control group, which could be an explanation for the decrease in GI and PD. However, Demirturk-Gocgun et al.³² found significant improvement in PI and PD one month following SRP adjuvant LLLT in patients with NIDDM. While, Crispino et al.³³ mentioned that diode LILT in addition to SRP was associated with more evident results in periodontal parameters (GI, PI and PD) of CP patients. Moreover, Obradović  et al.³⁴ proved that LLLT improved healing of gingival tissue as evident of histologic findings and absence of inflammatory cells.

Regarding glycemic control, our findings revealed significantly reduced level of HBA1c  that indicated improvement in glycemic control after 3 months of scaling and root planing, adjuvant LLLT, while many studies indicated that periodontal therapy resulted in low level of HBA1c in NIDDM patients.^35‒37 While, Stewart et al.³⁵ stated that nine months of periodontal treatment significantly improved glucose control in NIDDM patients.³⁸ However, Yun et al.³⁹ reported reduction in glycated hemoglobin (HbAlc), plaque index and bleeding on probing scores after 16 weeks of SRP in 46 NIDDM patients with CP.³⁹ Similarly, Botero  et al.⁴⁰ mentioned that their  systematic review proved that 3 months of periodontal treatment in NIDDM patients with CP. Moreover, Kocak et al.⁴¹ proved that 3 months of LILT in addition to SRP significantly reduced HbA1c in type 2 diabetics with periodontitis.

The possible mechanisms for the positive effects of combining laser therapy with SRP were  achieved via  more effective decontamination and slower recolonization of the pocket.^42‒44 However, the curettage effect of laser ensure complete removal of infected sulcular epithelium.^45,46 While, infected granulation tissue removal induce connective tissue healing that minimize the GI and PD.^47‒51 In addition to the diode laser antimicrobial effect that kills the periodontal microorganism.⁵¹ In the other hand, laser accelerates mitochondrial production of adenosine triphosphate (ATP) through respiratory chain system biomodulative effect which induce halving of cell duplication times.^52,53

Low intensity laser therapy as an effective adjunct to periodontal therapy upon periodontal inflammation in NIDDM Saudi patients with CP.

None.

None.

Author declares that there is no conflict of interest.

1. Cullinan MP, Ford PJ, Seymour GJ. Periodontal disease and systemic health: current status. Aust Dent J. 2009;54:1S62–S69.
2. Papapanou PN, Sanz M, Buduneli N, et al. Greenwell, Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri‐implant diseases and conditions. J Periodontol. 2018;89:S173–S82.
3. Taylor JJ, Preshaw PM, Lalla E, et al. A review of the evidence for pathogenicmechanisms that may link periodontitis and diabetes. J Clin Periodontol. 2013;40 Suppl 14:S113–S134.
4. Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship, Diabetol. 2012;55(1):21–31.
5. Loe H. Periodontal disease. The sixth complication of diabetes. Diabetes Care. 1993;16(1):329–334.
6. D'Aiuto F, Gkranias N, Bhowruth D, et al. Systemic effects of periodontitis treatment in patients with type 2 diabetes: a 12 month, single-centre, investigator-masked, randomised trial. Lancet Diabetes Endocrinol. 2018;6(12):954‒965.
7. Cobb CM. Clinical significance of non-surgical periodontal therapy: an evidence-based perspective of scaling and root planning. J Clin Periodontol. 2002;29 Suppl 2:6–16.
8. Agossa K, Morand DN, Tenenbaum H, et al. Systemic application of anti-inflammatory agents in periodontal treatment. Clinical Anti-Inflammatory & Anti-Allergy Drugs. 2016;2(1):3–13.
9. Akram Z, Abduljabbar T, Kellesarian SV, et al. Efficacy of bisphosphonate as an adjunct to nonsurgical periodontal therapy in the management of periodontal disease: a systematic review. Br J Clin Pharmacol. 2017;83(3):444‒454.
10. Alshammari A, Patel J, Al-Hashemi J, et al. “Kava-241 reduced periodontal destruction in a collagen antibody primed Porphyromonas gingivalis model of periodontitis. J Clin Periodontol. 2017;44(11):1123–1132.
11. Gokhale SR, Padhye AM. Future prospects of systemic host modulatory agents in periodontal therapy. British Dental Journal. 2013;214(9):467–471.
12. Martin-Cabezas R, Davideau JL, Tenenbaum H, et al. Clinical efficacy of probiotics as an adjunctive therapy to non-surgical periodontal treatment of chronic periodontitis: a systematic review and meta-analysis. Journal of Clinical Periodontology. 2016;43(6):520–530.
13. Gundogar H, Senyurt SZ, Erciyas K, et al. The effect oflow-level laser therapy on non-surgical periodontal treatment: a randomizedcontrolled, single-blind, split-mouth clinical trial. Lasers Med Sci. 2016;31(9):1767–1773.
14. Farivar S, Malekshahabi T, Shiari R. Biological effects of low level laser therapy. J Lasers Med Sci. 2014;5(2):58–62.
15. Caruso U, Nastri L, Piccolomini R, et al. Use of diode laser 980 nm as adjunctive therapy in the treatment of chronic periodontitis. A randomized controlled clinical trial. New Microbiol. 2008;31(4):513‒518.
16. Convissar RA. Principles and practice of laser dentistry: Elsevier Health Sciences; 2015. 328 p.
17. Bortone F, Santos HA, Albertini R, et al. Low level laser therapy modulates kinin receptors mRNA expression in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation. Int Immunopharmacol. 2008;8(2):206–210.
18. Obradovic R, Kesic L, Mihailovic D, et al. A histological evaluation of a low level laser therapy as an adjunct to periodontal therapy in patients with diabetes mellitus. Lasers Med Sci. 2013;28(1):19–24.
19. Crispino A, Figliuzzi MM, Iovane C, et al. Effectiveness of a diode laser in addition to non-surgical periodontal therapy: study of intervention. Ann Stomatol (Roma). 2015;6(1):15‒20.
20. Segarra-Vidal M, Guerra-Ojeda S, Vallés LS, et al. Effects of photodynamic therapy in periodontal treatment: A randomized, controlled clinical trial. J Clin Periodontol. 2017;44(9):915‒925.
21. Soskolne WA, Klinger A. The relationship between periodontal diseases and diabetes: an overview. Ann Periodontol. 2001;6(1):91–98.
22. Loe H. Periodontal disease: the sixth complication of diabetes mellitus. Diab Care. 1993;16(1):329–334.
23. Al Mubarak S, Rass MA, Alsuwyed A, et al. A new paradigm between mechanical scaling and root planing combined with adjunctive chemotherapy for glycated hemoglobin improvement in diabetics. Int J Diab Mellitus. 2010;2(3):158–164.
24. Sun WL, Chen LL, Zhang SZ, et al. Inflammatory cytokines, adiponectin, insulin resistance and metabolic control after periodontal intervention in patients with type 2 diabetes and chronic periodontitis. Intern Med. 2011;50(15):1569–1574.
25. Kocak E, Saglam M, Kayis SA, et al. Nonsurgical periodontal therapy with/without diode laser modulates metabolic control of type 2 diabetics with periodontitis: a randomized clinical trial. Lasers Med Sci. 2016;31(2):343–353.
26. Calderin S, Garcia-Nunez JA, Gomez C, et al. Short-term clinical and osteoimmunological effects of scaling and root planing complemented by simple or repeated laser phototherapy in chronic periodontitis. Lasers Med Sci. 2013;28(1):157–166.
27. Gundogar H, Senyurt SZ, Erciyas K, et al. The effect of low-level laser therapy on non-surgical periodontal treatment: a randomized controlled, single-blind, split-mouth clinical trial. Lasers Med Sci. 2016;31(9):1767–1773.
28. Ustun K, Erciyas K, Sezer U, et al. Clinical and biochemical effects of 810 nm diode laser as an adjunct to periodontal therapy: a randomized split-mouth clinical trial. Photomed Laser Surg. 2014;32(2):61–66.
29. Lee JH, Chiang MH, Chen PH, et al. Anti-inflammatory effects of low-level laser therapy on human periodontal ligament cells: in vitro study. Lasers Med Sci. 2018;33(3):469‒477.
30. Kellesarian SV, Malignaggi VR, Majoka HA, A et al. Effect of laser-assisted scaling and root planing on the expression of pro-inflammatory cytokines in the gingival crevicular fluid of patients with chronic periodontitis: A systematic review. Photodiagnosis Photodyn Ther. 2017;18:63‒77.
31. Ustun K, Erciyas K, Sezer U, et al. Clinical and biochemical effects of 810 nm diode laser as an adjunct to periodontal therapy: a randomized split-mouth clinical trial. Photomed Laser Surg. 2014;32(2):61‒66.
32. Demirturk-Gocgun O, Baser U, Aykol-Sahin G, et al. 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. Photomed Laser Surg. 2017;35(2):111‒115.
33. Crispino A, Figliuzzi MM, Iovane C, et al. Effectiveness of a diode laser in addition to non-surgical periodontal therapy: study of intervention. Ann Stomatol (Roma). 2015;6(1):15‒20.
34. Obradović R, Kesić L, Mihailović D, et al. A histological evaluation of a low-level laser therapy as an adjunct to periodontal therapy in patients with diabetes mellitus. Lasers Med Sci. 2013;28(1):19‒24.
35. Kiran M, Arpak N, Unsal E, et al. Effect of improved periodontal health on metabolic control in T2DM. J Clin Periodontol. 2005;32(3):266–272.
36. Navarro-Sanchez AB, Faria-Almeida R, Bascones-Martinez A. Effect of non-surgical periodontal therapy on clinical and immunological response and glycemic control in type 2 diabetic patients with moderate periodontitis. J Clin Periodontol. 2007;34(10):835–843.
37. Koromantzos PA, Makrilakis K, Dereka X, et al. A randomized, controlled trial on the effect of non-surgical periodontal therapy in patients with type 2 diabetes. Part I: effect on periodontal status and glycemic control. J Clin Periodontol. 2011;38(2):142–147.
38. Stewart JE, Wager KA, Friedlander AH, et al. The effect of periodontal treatment on glycemic control in patients with type 2 diabetes mellitus. J Clin Periodontol. 2001;28(4):306–310.
39.  Yun D, Firkova EI, Lin JQ, et al. Effect of non-surgical periodontal therapy on patients with type 2 diabetes mellitus. Folia Med (Plovdiv). 2007;49(1-2):32‒36.
40. Botero JE, Rodríguez C, Agudelo-Suarez AA. Periodontal treatment and glycaemic control in patients with diabetes and periodontitis: an umbrella review. Aust Dent J. 2016;61(2):134‒148.
41. Koçak E, Sağlam M, Kayış SA, et al. Nonsurgical periodontal therapy with/without diode laser modulates metabolic control of type 2 diabetics with periodontitis: a randomized clinical trial. Laser Med Sci. 2016;31(2):343‒353.
42. Moritz A, Gutknecht N, Doertbudak O, et al. Bacterial reduction in periodontal pockets through irradiation with a diode laser: a pilot study. J Clin Laser Med Surg. 1997;15(1):33‒37.
43. Moritz A, Schoop U, Goharkhay K, et al. Treatment of periodontal pockets with a diode laser. Lasers Surg Med. 1998;22(5):302‒311.
44. Saglam M, Kantarci A, Dundar N, et al. Clinical and biochemical effects of diode laser as an adjunct to nonsurgical treatment of chronic periodontitis: a randomized, controlled clinical trial. Lasers Med Sci. 2014;29(1):37‒46.
45. Kamma JJ, Vasdekis VG, Romanos GE. The effect of diode laser (980 nm) treatment on aggressive periodontitis: evaluation of microbial and clinical parameters. Photomed Laser Surg. 2009;27(1):11‒19.
46. 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(5):350‒355.
47. Angelov N, Pesevska S, Nakova M, et al. Periodontal treatment with a low-level diode laser: clinical findings. Gen Dent. 2009;57(5):510‒513.
48. Caruso U, Nastri L, Piccolomini R, et al. Use of diode laser 980 nm as adjunctive therapy in the treatment of chronic periodontitis. A randomized controlled clinical trial. New Microbiol. 2008;31(4):513‒518.
49. Giannelli M, Formigli L, Lorenzini L, et al. Combined photoablative and photodynamic diode laser therapy as an adjunct to non-surgical periodontal treatment. A randomized splitmouth clinical trial. J Clin Periodontol. 2012;39(10):962‒970.
50. Pejcic A, Kojovic D, Kesic L, et al. The effects of low level laser irradiation on gingival inflammation. Photomed Laser Surg. 2010;28(1):69‒74.
51. Gojkov-Vukelic M, Hadzic S, Dedic A, et al. Application of a diode laser in the reduction of targeted periodontal pathogens. Acta Inform Med. 2013;21(4):237‒240.
52. Passarella S, Casamassima E, Molinari S, et al. Increase of proton electrochemical potential and ATPsynthesis in rat liver mitochondria irradiated in vitro by helium-neon laser. FEBS Lett. 1984;175(1):95–99.
53. Benedicenti S, Pepe IM, Angiero F, et al. Intracellular ATP level increases in lymphocytes irradiated with infrared laser light of wavelength 904 nm. Photomed Laser Surg. 2008;26(5):451‒453.