Nonsurgical periodontal treatment improved the type 2 diabetes mellitus status in smokers: A randomized controlled trial

Published:November 11, 2022DOI:


      • There was significant improvement in the periodontal status in smokers after NSPT for up to 6 months.
      • There were significant reductions in metabolic parameters and pro-inflammatory markers in smokers after NSPT for up to 6 months.
      • Smokers not treated with NSPT showed slight increases in metabolic parameters and pro-inflammatory markers.



      Type 2 diabetes mellitus (T2D) and periodontal disease have bilateral associations. The effect of periodontal treatment on T2D patients who smoke is scarce. This study aimed to assess the effect of nonsurgical periodontal treatment (NSPT) in periodontitis smokers with T2D for a duration of 6 months of follow-up.

      Materials and methods

      Forty moderate to severe periodontitis smokers with T2D were randomly distributed into two different treatment groups: the test group (NSPT including oral hygiene instructions, scaling and root planing; and 0.05% Chlorhexidine mouthrinse) and the control group (treatment including oral hygiene instructions, supragingival removal of plaque and calculus and 0.05% Chlorhexidine mouthrinse). Periodontal parameters including plaque index (PI), gingival index (GI), bleeding on probing (BOP), periodontal probing depth (PPD) and clinical attachment loss (CAL) were examined. Metabolic parameters, including fasting plasma glucose (FPG) and glycated hemoglobin (HbA1c), and high-sensitivity C-reactive protein (hs-CRP) were evaluated at baseline and at 1, 3, and 6 months of follow-up.


      The test group significantly improved all periodontal parameters and reduced metabolic parameters and hs-CRP, whereas improvements in PI and GI were observed in the control group at 1, 3 and 6 months of follow-up. However, the PPD, CAL, metabolic parameters and hs-CRP increased in the control group at 3 and 6 months of follow-up, but the differences were not significant.


      NSPT improves the periodontal status of smokers with T2D, has a favorable effect on glycemic control and reduces pro-inflammatory mediators, which may limit complications due to T2D in these patients.


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        • Oliver R.C.
        • Brown L.J.
        • Loe H.
        Periodontal diseases in the United States population.
        J Periodontol. 1998; 69: 269-278
        • Verhulst M.JL.
        • Loos B.G.
        • Gerdes V.EA.
        • Teeuw W.J.
        Evaluating All Potential Oral Complications of Diabetes Mellitus.
        Front Endocrinol (Lausanne). 2019; 10: 56
        • Casanova L.
        • Hughes F.J.
        • Preshaw P.M.
        Diabetes and periodontal disease: a two-way relationship.
        Br Dent J. 2004; 217: 433-437
        • Stöhr J.
        • Barbaresko J.
        • Neuenschwander M.
        • Schlesinger S.
        Bidirectional association between periodontal disease and diabetes mellitus: a systematic review and meta-analysis of cohort studies.
        Sci Rep. 2021; 11: 13686
        • Pham T.A.V.
        • Tran T.T.P.
        The interaction among obesity, type 2 diabetes mellitus, and periodontitis in Vietnamese patients.
        Clin Exp Dent Res. 2018; 4: 63-71
        • Stratton I.M.
        • Adler A.I.
        • Neil H.A.
        • Matthews D.R.
        • Manley S.E.
        • Cull C.A.
        • et al.
        Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes: prospective observational study.
        BMJ. 2000; 321: 405-412
        • Taylor G.W.
        • Borgnakke W.S.
        Periodontal disease: Associations with diabetes, glycemic control and complications.
        Oral Dis. 2008; 14: 191-203
        • Hasan S.M.M.
        • Rahman M.
        • Nakamura K.
        • Tashiro Y.
        • Miyashita A.
        • Seino K.
        Relationship between diabetes self-care practices and control of periodontal disease among type2 diabetes patients in Bangladesh.
        PLoS ONE. 2021; 16e0249011
        • Makkar H.
        • Reynolds M.A.
        • Wadhawan A.
        • Dagdag A.
        • Merchant A.T.
        • Postolache T.T.
        Periodontal, metabolic, and cardiovascular disease: Exploring the role of inflammation and mental health.
        Pteridines. 2018; 29: 124-163
        • Wu T.
        • Trevisan M.
        • Genco R.J.
        • Falkner K.L.
        • Dorn J.P.
        • Sempos C.T.
        Examination of the relation between periodontal health status and cardiovascular risk factors: serum total and high density lipoprotein cholesterol, C-reactive protein, and plasma fibrinogen.
        Am J Epidemiol. 2000; 151: 273-282
        • Raman R.P.C.
        • Taiyeb-Ali T.B.
        • Chan S.P.
        • Chinna K.
        • Vaithilingam R.D.
        Effect of nonsurgical periodontal therapy verses oral hygiene instructions on Type 2 diabetes subjects with chronic periodontitis: a randomized clinical trial.
        BMC Oral Health. 2014; 14: 79
        • Pham T.A.V.
        • Kieu T.Q.
        • Ngo L.T.Q.
        Risk factors of periodontal disease in Vietnamese patients.
        J Investig Clin Dent. 2018; 9
        • Türkoğlu O.
        • Eren G.
        • Emingil G.
        • Azarsız E.
        • Kutukculer N.
        • Atilla G.
        Does smoking affect gingival crevicular fluid LL-37 levels following non-surgical periodontal treatment in chronic periodontitis?.
        Arch Oral Biol. 2016; 61: 98-105
        • Kinane D.F.
        • Stathopoulou P.G.
        • Papapanou P.N.
        Periodontal diseases Nat Rev Dis Primers. 2017; 3: 17038
      1. U.S. Department of Health and Human Services. The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, 2014; Chapter 10: 537-545.

        • Chang S.A.
        Smoking and Type 2 diabetes mellitus.
        Diabetes Metab J. 2012; 36: 399-403
        • Battancs E.
        • Gheorghita D.
        • Nyiraty S.
        • Lengyel C.
        • Eördegh G.
        • Baráth Z.
        • et al.
        Periodontal disease in diabetes mellitus: A case–control study in smokers and non-smokers.
        Diabetes Ther. 2020; 11: 2715-2728
        • Sun W.L.
        • Chen L.L.
        • Zhang S.Z.
        • Wu Y.M.
        • Ren Y.Z.
        • Qin G.M.
        Inflammatory cytokines, adiponectin, insulin resistance and metabolic control after periodontal intervention in patients with type 2 diabetes and chronic periodontitis.
        Intern Med. 2011; 50: 1569-1574
        • Teshome A.
        • Yitayeh A.
        The effect of periodontal therapy on glycemic control and fasting plasma glucose level in type 2 diabetic patients: systematic review and meta-analysis.
        BMC Oral Health. 2016; 17: 31
        • Pham N.M.
        • Eggleston K.
        Diabetes prevalence and risk factors among Vietnamese adults: findings from community-based screening programs.
        Diabetes Care. 2015; 38: E77-E78
      2. WHO. Smoking causes 40 000 deaths in Viet Nam each year. Vietnam: World Health Organization, 27 May 2018 [Google Scholar].

      3. IDF. Clinical guidelines task force. Global guideline for type 2 diabetes. Brussels: International Diabetes Federation, 2005. [Google Scholar].

        • World Health Organization
        Preventing and managing the global epidemic.
        Report of a who consultation on obesity, Geneva1998
        • American Academy of Periodontology
        Task force report on the update to the 1999 classification of periodontal diseases and conditions.
        J Periodontol. 2015; 86: 835-838
        • Teeuw W.J.
        • Gerdes V.E.
        • Loos B.G.
        Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and meta-analysis.
        Diabetes Care. 2010; 33: 421-427
        • Loe H.
        The Gingival Index, the Plaque Index and the Retention Index Systems.
        J Periodontol. 1967; 38: 610-616
        • Van der Weijden G.A.
        • Timmerman M.F.
        • Nijboer A.
        • Reijerse E.
        • Van der Velden U.
        Comparison of different approaches to assess bleeding on probing as indicators of gingivitis.
        J Clin Periodontol. 1994; 21: 589-594
        • Chen L.
        • Luo G.
        • Xuan D.
        • Bihong Wei B.
        • Liu F.
        • Li J.
        • et al.
        Effects of non-surgical periodontal treatment on clinical response, serum inflammatory parameters, and metabolic control in patients with type 2 diabetes: a randomized study.
        J Periodontol. 2012; 83: 435-443
        • Koromantzos P.A.
        • Makrilakis K.
        • Dereka X.
        • Katsilambros N.
        • Vrotsos I.A.
        • Madianos P.N.
        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 glycaemic control.
        J Clin Periodontol. 2011; 38: 142-147
        • Mauri-Obradors E.
        • Merlos A.
        • Estrugo-Devesa A.
        • Jané-Salas E.
        • López-López J.
        • Viñas M.
        Benefits of nonsurgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: a randomized controlled trial.
        J Clin Periodontol. 2018; 45: 345-353
        • Kaur P.K.
        • Narula S.C.
        • Rajput R.K.
        • Sharma R.
        • Tewari S.
        Periodontal and glycemic effects of nonsurgical periodontal therapy in patients with type 2 diabetes stratified by baseline HbA1c.
        J Oral Sci. 2015; 57: 201-211
        • Liew A.K.C.
        • Punnanithinont N.
        • Lee Y.C.
        • Lee Y.C.
        • Yang J.
        Effect of non-surgical periodontal treatment on HbA1c: A meta-analysis of randomized controlled trials.
        Aust Dent J. 2013; 58: 350-357
      4. D'Aiuto F, Gkranias N, Bhowruth D, Khan T, Orlandi M, Suvan J, Masi S, Tsakos G, Hurel S, Hingorani AD, Donos N, Deanfield JE; TASTE Group. 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.

        • Correa F.O.
        • Gonçalves D.
        • Figueredo C.M.
        • Bastos A.S.
        • Gustafsson A.
        • Orrico S.R.
        Effect of periodontal treatment on metabolic control, systemic inflammation and cytokines in patients with type 2 diabetes.
        J Clin Periodontol. 2010; 37: 53-58
        • Telgi R.L.
        • Tandon V.
        • Tangade P.S.
        • Tirth A.
        • Kumar S.
        • Yadav V.
        Efficacy of nonsurgical periodontal therapy on glycaemic control in type II diabetic patients: a randomized controlled clinical trial.
        J Periodontal Implant Sci. 2013; 43: 177-182
        • Kiran M.
        • Arpak N.
        • Unsal E.
        • Erdogan M.F.
        The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus.
        J Clin Periodontol. 2005; 32: 266-272
        • Machado V.
        • Botelho J.
        • Escalda C.
        • Hussain S.B.
        • Luthra S.
        • Mascarenhas P.
        • et al.
        Serum C-reactive protein and periodontitis: a systematic review and meta-analysis.
        Front Immunol. 2021; 12706432
        • Katagiri S.
        • Nitta H.
        • Nagasawa T.
        • Uchimura I.
        • Izumiyama H.
        • Inagaki K.
        • et al.
        Multi-center intervention study on glycohemoglobin (HbA1c) and serum, high-sensitivity CRP (hs-CRP) after local anti-infectious periodontal treatment in Type 2 diabetic patients with periodontal disease.
        Diabetes Res Clin Pract. 2009; 83: 308-315
        • Lalla E.
        • Kaplan S.
        • Yang J.
        • Roth G.A.
        • Papapanou P.N.
        • Greenberg S.
        Effects of periodontal therapy on serum C-reactive protein, sE-selectin, and tumor necrosis factor-alpha secretion by peripheral blood-derived macrophages in diabetes.
        A pilot study J Periodontal Res. 2007; 42: 274-282
        • D’Aiuto F.
        • Nibali L.
        • Parkar M.
        • Suvan J.
        • Tonetti M.S.
        Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol.
        J Dent Res. 2005; 84: 269-273
      5. Del Cañizo Gómez FJ, Fernández Pérez C, Moreno Ruiz I, Pérez-Jáuregui CG, Rodríguez BS, Losada TG, Galindo AS. Microvascular complications and risk factors in patients with Type 2 diabetes. Endocrinol Nutr 2011; 58 (4): 163-168.