Association of periodontal disease with glycemic control in patients with type 2 diabetes in Indian population

Abstract

This study aims to investigate the link between glycated hemoglobin and diabetic complications with chronic periodontitis. A total of 207 patients with type 2 diabetes and chronic periodontitis (CP) were divided according to tertiles of mean PISA (periodontal inflamed surface area) scores as low, middle and high PISA groups. Simultaneously a group of 67 periodontally healthy individuals (PH) was recruited. Periodontal examinations, including full-mouth assessment of probing depths (PPD), bleeding on probing, clinical attachment level and plaque scores were determined. Blood analyses were carried out for glycated hemoglobin (HbA_1c), fasting plasma glucose (FPG), 2 h post parandial glucose (PPG). Individuals in PH group had significantly better glycemic control than CP group. Upon one-way analysis of variance, subjects with increased PISA had significantly higher HbA_1c levels, retinopathy and nephropathy (P<0.05). After controlling for age, gender, body mass index (BMI), socioeconomic status (SES), family history of diabetes and periodontitis, duration of diabetes, the mean PISA in mm², PPD 4--6 mm (%) and PPD≥7 mm (%) emerged as significant predictors for elevated HbA_1c in regression model (P<0.05). Logistic regression analysis revealed that PISA was associated with higher risk of having retinopathy and neuropathy (odds ratio). In our study, the association between glycemic control and diabetic complications with periodontitis was observed.

Keywords

type 2 diabetes mellitus / hemoglobin A / glycated / chronic periodontitis

References

[1] Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 2013; 40(Suppl 14): S113–S134

[2] King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol 2008; 79(8Suppl ): 1527–1534

[3] Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Front Biosci 2008; 13(13): 1227–1239

[4] Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005; 366(9499): 1809–1820

[5] Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993; 16(1): 329–334

[6] Garcia RI, Henshaw MM, Krall EA. Relationship between periodontal disease and systemic health. Periodontol 2000 2001; 25(1): 21–36

[7] Amar S, Han X. The impact of periodontal infection on systemic diseases. Med Sci Monit 2003; 9(12): RA291–RA299

[8] Lu HK, Yang PC. Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent 2004; 24(1): 71–79

[9] Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: a case-control study. J Periodontol 2005; 76(3): 418–425

[10] Lu HK, Yang PC. Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent 2004; 24(1): 71–79

[11] Novak KF, Taylor GW, Dawson DR, Ferguson JE 2nd, Novak MJ. Periodontitis and gestational diabetes mellitus: exploring the link in NHANES III. J Public Health Dent 2006; 66(3): 163–168

[12] Novak MJ, Potter RM, Blodgett J, Ebersole JL. Periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol 2008; 79(4): 629–636

[13] Wang TT, Chen TH, Wang PE, Lai H, Lo MT, Chen PY, Chiu SY. A population-based study on the association between type 2 diabetes and periodontal disease in 12,123 middle-aged Taiwanese (KCIS No. 21). J Clin Periodontol 2009; 36(5): 372–379

[14] Rajhans NS, Kohad RM, Chaudhari VG, Mhaske NH. A clinical study of the relationship between diabetes mellitus and periodontal disease. J Indian Soc Periodontol 2011; 15(4): 388–392

[15] Pathak AK, Shakya VK, Chandra A, Goel K. Association between diabetes mellitus and periodontal status in north Indian adults. European J Gen Dent 2013; 2(1): 58–61

[16] Kalra N, Pradeep AR, Priyanka N, Kumari M. Association of stem cell factor and high-sensitivity C reactive protein concentrations in crevicular fluid and serum in patients with chronic periodontitis with and without type 2 diabetes. J Oral Sci 2013; 55(1): 57–62

[17] Tandon V, Tangade P, Lingesha RT, Tirth A, Pal SK, Yadav V. Glycemic control and periodontal disease in type 2 diabetes mellitus patients: a cross-sectional study. J Indian Assoc Public Health Dent 2015; 13(3): 297–301

[18] Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol 1996; 67(10 Suppl): 1085–1093

[19] Noma H, Sakamoto I, Mochizuki H, Tsukamoto H, Minamoto A, Funatsu H, Yamashita H, Nakamura S, Kiriyama K, Kurihara H, Mishima HK. Relationship between periodontal disease and diabetic retinopathy. Diabetes Care 2004; 27(2): 615

[20] Taylor GW, Borgnakke WS. Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis 2008; 14(3): 191–203

[21] Nesse W, Linde A, Abbas F, Spijkervet FK, Dijkstra PU, de Brabander EC, Gerstenbluth I, Vissink A. Dose-response relationship between periodontal inflamed surface area and HbA1c in type 2 diabetics. J Clin Periodontol 2009; 36(4): 295–300

[22] Abrao L, Chagas JK, Schmid H. Periodontal disease and risk for neuropathic foot ulceration in type 2 diabetes. Diabetes Res Clin Pract 2010; 90(1): 34–39

[23] Chen L, Wei B, Li J, Liu F, Xuan D, Xie B, Zhang J. Association of periodontal parameters with metabolic level and systemic inflammatory markers in patients with type 2 diabetes. J Periodontol 2010; 81(3): 364–371

[24] Morita T, Yamazaki Y, Mita A, Takada K, Seto M, Nishinoue N, Sasaki Y, Motohashi M, Maeno M. A cohort study on the association between periodontal disease and the development of metabolic syndrome. J Periodontol 2010; 81(4): 512–519

[25] Demmer RT, Desvarieux M, Holtfreter B, Jacobs DR Jr, Wallaschofski H, Nauck M, Völzke H, Kocher T. Periodontal status and A1C change: longitudinal results from the study of health in Pomerania (SHIP). Diabetes Care 2010; 33(5): 1037–1043

[26] Susanto H, Nesse W, Dijkstra PU, Hoedemaker E, van Reenen YH, Agustina D, Vissink A, Abbas F. Periodontal inflamed surface area and C-reactive protein as predictors of HbA1c: a study in Indonesia. Clin Oral Investig 2012; 16(4): 1237–1242

[27] Southerland JH, Moss K, Taylor GW, Beck JD, Pankow J, Gangula PR, Offenbacher S. Periodontitis and diabetes associations with measures of atherosclerosis and CHD. Atherosclerosis 2012; 222(1): 196–201

[28] Kim EK, Lee SG, Choi YH, Won KC, Moon JS, Merchant AT, Lee HK. Association between diabetes-related factors and clinical periodontal parameters in type-2 diabetes mellitus. BMC Oral Health 2013; 13: 64PMID:24195646

[29] Casanova L, Hughes FJ, Preshaw PM. Diabetes and periodontal disease: a two-way relationship. Br Dent J 2014; 217(8): 433–437

[30] Amiri AA, Maboudi A, Bahar A, Farokhfar A, Daneshvar F, Khoshgoeian HR, Nasohi M, Khalilian A. Relationship between type 2 diabetic retinopathy and periodontal disease in Iranian adults. N Am J Med Sci 2014; 6(3): 139–144

[31] Gokhale NH, Acharya AB, Patil VS, Trivedi DJ, Setty S, Thakur SL. Resistin levels in gingival crevicular fluid of patients with chronic periodontitis and type 2 diabetes mellitus. J Periodontol 2014; 85(4): 610–617

[32] Simpson TC, Weldon JC, Worthington HV, Needleman I, Wild SH, Moles DR, Stevenson B, Furness S, Iheozor-Ejiofor Z. Treatment of periodontal disease for glycaemic control in people with diabetes mellitus. Cochrane Database Syst Rev 2015; 11(11): CD004714

[33] 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(2): 421–427

[34] Liew AK, Punnanithinont N, Lee YC, Yang J. Effect of non-surgical periodontal treatment on HbA1c: a meta-analysis of randomized controlled trials. Aust Dent J 2013; 58(3): 350–357

[35] Engebretson S, Kocher T. Evidence that periodontal treatment improves diabetes outcomes: a systematic review and meta-analysis. J Periodontol 2013; 84(4 Suppl): S153–S169

[36] Sgolastra F, Severino M, Pietropaoli D, Gatto R, Monaco A. Effectiveness of periodontal treatment to improve metabolic control in patients with chronic periodontitis and type 2 diabetes: a meta-analysis of randomized clinical trials. J Periodontol 2013; 84(7): 958–973

[37] Mohan M, Jhingran R, Bains VK, Gupta V, Madan R, Rizvi I, Mani K. Impact of scaling and root planing on C-reactive protein levels in gingival crevicular fluid and serum in chronic periodontitis patients with or without diabetes mellitus. J Periodontal Implant Sci 2014; 44(4): 158–168

[38] Bhopal R, Rankin J. Concepts and terminology in ethnicity, race and health: be aware of the ongoing debate. Br Dent J 1999; 186(10): 483–484

[39] Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol 2007; 78(7 Suppl): 1387–1399

[40] Costa FO, Guimarães AN, Cota LO, Pataro AL, Segundo TK, Cortelli SC, Costa JE. Impact of different periodontitis case definitions on periodontal research. J Oral Sci 2009; 51(2): 199–206

[41] 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(5): 385–397

[42] Nesse W, Abbas F, van der Ploeg I, Spijkervet FKL, Dijkstra PU, Vissink A. Periodontal inflamed surface area: quantifying inflammatory burden. J Clin Periodontol 2008; 35(8): 668–673

[43] American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010; 33(Suppl 1): S62–S69

[44] Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964; 22(1): 121–135

[45] Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963; 21(6): 533–551

[46] Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol 1996; 67(10 Suppl): 1041–1049

[47] Torrungruang K, Tamsailom S, Rojanasomsith K, Sutdhibhisal S, Nisapakultorn K, Vanichjakvong O, Prapakamol S, Premsirinirund T, Pusiri T, Jaratkulangkoon O, Unkurapinun N, Sritara P. Risk indicators of periodontal disease in older Thai adults. J Periodontol 2005; 76(4): 558–565

[48] Choi BC, Shi F. Risk factors for diabetes mellitus by age and sex: results of the National Population Health Survey. Diabetologia 2001; 44(10): 1221–1231

[49] Imrey PB. Considerations in the statistical analysis of clinical trials in periodontitis. J Clin Periodontol 1986; 13(5): 517–528

[50] Wolff RE, Wolff LF, Michalowicz BS. A pilot study of glycosylated hemoglobin levels in periodontitis cases and healthy controls. J Periodontol 2009; 80(7): 1057–1061

[51] Nibali L, D’Aiuto F, Griffiths G, Patel K, Suvan J, Tonetti MS. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case-control study. J Clin Periodontol 2007; 34(11): 931–937

[52] Kolb H, Mandrup-Poulsen T. The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation. Diabetologia 2010; 53(1): 10–20

[53] Engebretson S, Chertog R, Nichols A, Hey-Hadavi J, Celenti R, Grbic J. Plasma levels of tumour necrosis factor-α in patients with chronic periodontitis and type 2 diabetes. J Clin Periodontol 2007; 34(1): 18–24

[54] Paraskevas S, Huizinga JD, Loos BG. A systematic review and meta-analyses on C-reactive protein in relation to periodontitis. J Clin Periodontol 2008; 35(4): 277–290

[55] Ebrahimi A, Nabipour I, Vahdat K, Jafari SM, Fouladvand M, Assadi M, Movahed A, Obeidi N, Sanjdideh Z. High sensitivity C-reactive protein is associated with the metabolic syndrome independent to viral and bacterial pathogen burden. Diabetes Res Clin Pract 2009; 84(3): 296–302

[56] Hung CH, Lee CM, Chen CH, Hu TH, Jiang SR, Wang JH, Lu SN, Wang PW. Association of inflammatory and anti-inflammatory cytokines with insulin resistance in chronic hepatitis C. Liver Int 2009; 29(7): 1086–1093

[57] Hujoel PP, Drangsholt M, Spiekerman C, DeRouen TA. Periodontitis-systemic disease associations in the presence of smoking—causal or coincidental? Periodontol 2000 2002; 30(1): 51–60

Compliance with ethics guidelines

Palka Kaur Khanuja, Satish Chander Narula, Rajesh Rajput, Rajinder Kumar Sharma, and Shikha Tewari declare that there are no conflicts of interest in the study. All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.

RIGHTS & PERMISSIONS

2016 Higher Education Press and Springer-Verlag Berlin Heidelberg