Abstract
This review was designed to determine whether non-surgical periodontal treatment is able to reduce serum glycosylated hemoglobin (HbA1c) levels in patients with diabetes mellitus (DM). Several previous reports showed that scaling and root planning (SRP) improve periodontal status in patients with DM, but whether it also improves metabolic control of the disease is unclear. A systematic review was conducted according to the recommendations of the Cochrane Collaboration and PRISMA. A literature search was conducted in October 2012 using three libraries (Cochrane, Web of Knowledge, and Scopus) and the keywords “periodontal disease” and “diabetes mellitus.” Only 21 of the articles met the inclusion criteria for this review. A total of 1,454 patients were thus included in this study to evaluate whether periodontal treatment improved serum HbA1c levels. Both the methodological quality and the risk of bias of each study were taken into account using the Jadad scale. Only ten of the included studies had an acceptable–good score of 3–5. Fourteen of the studies reported a significant decrease in serum HbA1c levels (p < 0.05) after periodontal treatment. The remaining seven studies failed to find a significant decrease in serum HbA1c. The findings of this review suggest that the published literature is insufficient and inconclusive to clearly support periodontal treatment as a means to improve serum HbA1c levels in patients with type 1 DM. It also demonstrates the need for homogeneous studies, with larger samples and longer follow-up periods, to properly address this question.
Similar content being viewed by others
References
King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol. 2008;79:1527–34.
The Diabetes Control and Complications Trial Research Group. The Effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J. 1993;329:977–86.
American Diabetes Association. Standards of medical care in diabetes. Diabetes Care. 2005;1:S4–42.
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2006;1:S43–8.
Kenny SJ, Aubert RE, Geiss LS. Prevalence and incidence of non-insulin-dependent diabetes. National Diabetes Data Group. In: Diabetes in America. 2nd ed. Bethesda, Md: National Institutes of Health, national Institute of Diabetes and Digestive and Kidney Diseases. IV47-68. NIH publication 1995; 95–1468.
Valdes S, Rojo-Martinez G, Soriguer F. Evolution of prevalence of type 2 diabetes in adult Spanish population. Med Clin. 2007;129:352–5.
Sammalkorpi K. Glucose intolerance in acute infections. J Intern Med. 1989;225:15–9.
Ebersole JL, Holt SC, Hansard R, Novak MJ. Microbiologic and immunologic characteristics of periodontal disease in Hispanic americans with type 2 diabetes. J Periodontol. 2008;79:637–46.
Grossi SG, Skrepcinski FB, DeCaro T, et al. Treatment of periodontal disease in diabetics reduces glycated hemoglobin. J Periodontol. 1997;68:713–9.
Lalla E. Periodontal infections and diabetes mellitus: when will the puzzle be complete? J Clin Periodontol. 2007;34:913–6.
Feingold KR, Grunfeld C. Role of cytokines in inducing hyperlipidemia. Diabetes. 1992;41:S97–101.
Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259:87–91.
Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286:327–34.
Wu T, Trevisan M, Genco RJ, Falkner KL, Dorn JP, Sempos CT. 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;151:273–82.
Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol. 2001;6:99–112.
López-López J, Jané-Salas E, Estrugo-Devesa A, Velasco-Ortega E, Martín-González J, Segura-Egea JJ. Periapical and endodontic status of type 2 diabetic patients in Catalonia, Spain: a cross-sectional study. J Endod. 2011;37:598–601.
Segura-Egea JJ, Castellanos-Cosano L, Machuca G, et al. Diabetes mellitus, periapical inflammation and endodontic treatment outcome. Med Oral Patol Oral Cir Bucal. 2012;17:e356–61.
Grossi SG, Genco RJ. Periodontal disease and diabetes mellitus: a two-way relationship. Ann Periodontol. 1998;3:51–61.
Iwamoto Y, Nishimura F, Nakagawa M, et al. The effect of antimicrobial periodontal treatment on circulating tumor necrosis factor-alpha and glycated hemoglobin level in patients with type 2 diabetes. J Periodontol. 2001;72:774–8.
Chen L, Luo G, Xuan D, 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;83:435–43.
Teeuw WJ, Gerdes VE, Loos BG. Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and meta-analysis. Diabetes Care. 2010;33:421–7.
Simpson TC, Needleman I, Wild SH, Moles, Mills EJ. Treatment of periodontal disease for glycaemic control in people with diabetes. Cochrane Database Syst Rev. 2010;12:CD004714.
Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 2011; The Cochrane Collaboration. Publishing PhysicsWeb. http://www.cochrane-handbook.org. Accedit 10/2012.
Urrutia G, Bonfill X. Prisma declaration: a proposal to improve the publication of systematic reviews and meta-analyses. Med Clin (Barc). 2010;135:507–11.
Manau C, Echeverria A, Agueda A, Guerrero A, Echeverria JJ. Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. J Clin Periodontol. 2008;35:385–97.
Moher D. Schulz KF, Altman DG; CONSORT Group. The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomised trials. Clin Oral Investig. 2003;7:2–7.
Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, McQuay HJ. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17:1–12.
Sun WL, Chen LL, Zhang SZ, Wu YM, Ren YZ, Qin GM. Inflammatory cytokines, adiponectin, insulin resistance and metabolic control after periodontal intervention in patients with type 2 diabetes and chronic periodontitis. Intern Med. 2011;50:1569–74.
Al-Zahrani MS, Bamshmous SO, Alhassani AA, Al-Sherbini MM. Short-term effects of photodynamic therapy on periodontal status and glycemic control of patients with diabetes. J Periodontol. 2009;80:1568–73.
Kiran M, Arpak N, Unsal E, Erdogan MF. The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus. J Clin Periodontol. 2005;32:266–72.
Al-Mubarak S, Ciancio S, Aljada A, Mohanty P, Ross C, Dandona P. Comparative evaluation of adjunctive oral irrigation in diabetics. J Clin Periodontol. 2002;29:295–300.
Rocha M. Nava LE, Vazquez de la Torre C, Sanchez-Marin F, Garay-Sevilla ME, Malacara JM. Clinical and radiological improvement of periodontal disease in patients with type 2 diabetes mellitus treated with alendronate: a randomized, placebo-controlled trial. J Periodontol. 2001;72:204–9.
O’Connell PA, Taba M, Nomizo A, et al. Effects of periodontal therapy on glycemic control and inflammatory markers. J Periodontol. 2008;79:774–83.
Koromantzos PA, Makrilakis K, Dereka X, Katsilambros N, Vrotsos IA, Madianos PN. 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;38:142–7.
Lin SJ, Tu YK, Tsai SC, Lai SM, Lu HK. Non-surgical periodontal therapy with and without subgingival minocycline administration in patients with poorly controlled type II diabetes: a randomized controlled clinical trial. Clin Oral Investig. 2012;16:599–609.
Moeintaghavi A, Arab HR, Bozorgnia Y, Kianoush K, Alizadeh M. Non-surgical periodontal therapy affects metabolic control in diabetics: a randomized controlled clinical trial. Aust Dent J. 2012;57:31–7.
Navarro-Sanchez AB, Faria-Almeida R, Bascones-Martinez A. Effect of non-surgical periodontal therapy on clinical and immunological response and glycaemic control in type 2 diabetic patients with moderate periodontitis. J Clin Periodontol. 2007;34:835–43.
Stewart JE, Wager KA, Friedlander AH, Zadeh HH. The effect of periodontal treatment on glycemic control in patients with type 2 diabetes mellitus. J Clin Periodontol. 2001;28:306–10.
Calabrese N, D’Aiuto F, Calabrese A, Patel K, Calabrese G, Massi-Benedetti M. Effects of periodontal therapy on glucose management in people with diabetes mellitus. Diabetes Metab. 2011;37:456–9.
Ou L, Li RF. Effect of periodontal treatment on glycosylated hemoglobin levels in elderly patients with periodontal disease and type 2 diabetes. Chin Med J (Engl). 2011;124:3070–3.
Kardesler L, Buduneli N, Cetinkalp S, Kinane DF. Adipokines and inflammatory mediators after initial periodontal treatment in patients with type 2 diabetes and chronic periodontitis. J Periodontol. 2010;81:24–33.
Promsudthi A, Pimapansri S, Deerochanawong C, Kanchanavasita W. The effect of periodontal therapy on uncontrolled type 2 diabetes mellitus in older subjects. Oral Dis. 2005;11:293–8.
Auyeung L, Wang PW, Lin RT, et al. Evaluation of periodontal status and effectiveness of non-surgical treatment in patients with type 2 diabetes mellitus in taiwan for a 1-year period. J Periodontol. 2012;83:621–8.
Santos VR, Lima JA, De Mendonca AC. Braz Maximo MB, Faveri M, Duarte PM. Effectiveness of full-mouth and partial-mouth scaling and root planing in treating chronic periodontitis in subjects with type 2 diabetes. J Periodontol. 2009;80:1237–45.
Katagiri S, Nitta H, Nagasawa T, 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;83:308–15.
Rodrigues DC, Taba MJ, Novaes AB, Souza SL, Grisi MF. Effect of non-surgical periodontal therapy on glycemic control in patients with type 2 diabetes mellitus. J Periodontol. 2003;74:1361–7.
Darre L, Vergnes JN, Gourdy P, Sixou M. Efficacy of periodontal treatment on glycaemic control in diabetic patients: a meta-analysis of interventional studies. Diabetes Metab. 2008;34:497–506.
Jones JA, Miller DR, Wehler CJ, Rich SE, Krall-Kaye EA, McCoy LC, Christinasen CL, Rothendler JA, García RI. Does periodontal care improve glycemic control? The Department of Veterans Affairs Dental Diabetes Study. J Clin Periodontol. 2007;34:46–52.
Borrell LN, Papapanou PN. Analytical epidemiology of periodontitis. J Clin Periodontol. 2005;32:S132–58.
Leach MJ, Kumar S. Cinnamon for diabetes mellitus. Cochrane Database Syst Rev 2012; 9:CD007170. doi: 10.1002/14651858.CD007170.pub2.
Janket SJ, Wightman A, Baird AE, Van Dyke TE, Jones JA. Does periodontal treatment improve glycemic control in diabetic patients? A meta-analysis of intervention studies. J Dent Res. 2005;84:1154–9.
Ainamo J, Lahtinen A, Uitto V. Rapid periodontal destruction in adult humans with poorly controlled diabetes. A report of 2 cases. J Clin Periodontol. 1990;17:22–8.
Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999;4:1–6.
Acknowledgments
This research was partially supported by Ajuts a la Recerca del Campus de Bellvitge UB. We thank Wendy Ran for assistance with copy editing the manuscript, and for comments that greatly improved the manuscript.
Conflict of interest
The authors deny any conflicts of interest or financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mauri-Obradors, E., Jané-Salas, E., Sabater-Recolons, M.M. et al. Effect of nonsurgical periodontal treatment on glycosylated hemoglobin in diabetic patients: a systematic review. Odontology 103, 301–313 (2015). https://doi.org/10.1007/s10266-014-0165-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10266-014-0165-2