Frontiers of Medicine

, Volume 11, Issue 1, pp 110–119 | Cite as

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

  • Palka Kaur KhanujaEmail author
  • Satish Chander Narula
  • Rajesh Rajput
  • Rajinder Kumar Sharma
  • Shikha Tewari
Research Article


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 (HbA1c), 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 HbA1c 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 HbA1c 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.


type 2 diabetes mellitus hemoglobin A glycated chronic periodontitis 


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  1. 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–S134PubMedGoogle Scholar
  2. 2.
    King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol 2008; 79(8Suppl ): 1527–1534CrossRefPubMedGoogle Scholar
  3. 3.
    Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Front Biosci 2008; 13(13): 1227–1239CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005; 366(9499): 1809–1820CrossRefPubMedGoogle Scholar
  5. 5.
    Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993; 16(1): 329–334CrossRefPubMedGoogle Scholar
  6. 6.
    Garcia RI, Henshaw MM, Krall EA. Relationship between periodontal disease and systemic health. Periodontol 2000 2001; 25(1): 21–36CrossRefPubMedGoogle Scholar
  7. 7.
    Amar S, Han X. The impact of periodontal infection on systemic diseases. Med Sci Monit 2003; 9(12): RA291–RA299PubMedGoogle Scholar
  8. 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): 71–79PubMedGoogle Scholar
  9. 9.
    Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: a case-control study. J Periodontol 2005; 76(3): 418–425CrossRefPubMedGoogle Scholar
  10. 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): 71–79PubMedGoogle Scholar
  11. 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): 163–168CrossRefPubMedGoogle Scholar
  12. 12.
    Novak MJ, Potter RM, Blodgett J, Ebersole JL. Periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol 2008; 79(4): 629–636CrossRefPubMedGoogle Scholar
  13. 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): 372–379CrossRefPubMedGoogle Scholar
  14. 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): 388–392CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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): 58–61CrossRefGoogle Scholar
  16. 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): 57–62CrossRefPubMedGoogle Scholar
  17. 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): 297–301CrossRefGoogle Scholar
  18. 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): 1085–1093CrossRefPubMedGoogle Scholar
  19. 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): 615CrossRefPubMedGoogle Scholar
  20. 20.
    Taylor GW, Borgnakke WS. Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis 2008; 14(3): 191–203CrossRefPubMedGoogle Scholar
  21. 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): 295–300CrossRefPubMedGoogle Scholar
  22. 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): 34–39CrossRefPubMedGoogle Scholar
  23. 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): 364–371CrossRefPubMedGoogle Scholar
  24. 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): 512–519CrossRefPubMedGoogle Scholar
  25. 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): 1037–1043CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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): 1237–1242CrossRefPubMedGoogle Scholar
  27. 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): 196–201CrossRefPubMedGoogle Scholar
  28. 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: 64CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Casanova L, Hughes FJ, Preshaw PM. Diabetes and periodontal disease: a two-way relationship. Br Dent J 2014; 217(8): 433–437CrossRefPubMedGoogle Scholar
  30. 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): 139–144CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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): 610–617CrossRefPubMedGoogle Scholar
  32. 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): CD004714Google Scholar
  33. 33.
    Teeuw WJ, Gerdes VE, Loos BG. Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and metaanalysis. Diabetes Care 2010; 33(2): 421–427CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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): 350–357CrossRefPubMedGoogle Scholar
  35. 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–S169PubMedPubMedCentralGoogle Scholar
  36. 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 metaanalysis of randomized clinical trials. J Periodontol 2013; 84(7): 958–973CrossRefPubMedGoogle Scholar
  37. 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): 158–168CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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): 483–484PubMedGoogle Scholar
  39. 39.
    Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol 2007; 78(7 Suppl): 1387–1399CrossRefPubMedGoogle Scholar
  40. 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): 199–206CrossRefPubMedGoogle Scholar
  41. 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): 385–397CrossRefPubMedGoogle Scholar
  42. 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): 668–673CrossRefPubMedGoogle Scholar
  43. 43.
    American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010; 33(Suppl 1): S62–S69CrossRefPubMedCentralGoogle Scholar
  44. 44.
    Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 1964; 22(1): 121–135CrossRefPubMedGoogle Scholar
  45. 45.
    Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 1963; 21(6): 533–551CrossRefPubMedGoogle Scholar
  46. 46.
    Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol 1996; 67(10 Suppl): 1041–1049CrossRefPubMedGoogle Scholar
  47. 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): 558–565CrossRefPubMedGoogle Scholar
  48. 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): 1221–1231CrossRefPubMedGoogle Scholar
  49. 49.
    Imrey PB. Considerations in the statistical analysis of clinical trials in periodontitis. J Clin Periodontol 1986; 13(5): 517–528CrossRefPubMedGoogle Scholar
  50. 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): 1057–1061CrossRefPubMedGoogle Scholar
  51. 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): 931–937CrossRefPubMedGoogle Scholar
  52. 52.
    Kolb H, Mandrup-Poulsen T. The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation. Diabetologia 2010; 53(1): 10–20CrossRefPubMedGoogle Scholar
  53. 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): 18–24CrossRefPubMedGoogle Scholar
  54. 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): 277–290CrossRefPubMedGoogle Scholar
  55. 55.
    Ebrahimi A, Nabipour I, Vahdat K, Jafari SM, Fouladvand M, Assadi M, Movahed A, Obeidi N, Sanjdideh Z. High sensitivity Creactive protein is associated with the metabolic syndrome independent to viral and bacterial pathogen burden. Diabetes Res Clin Pract 2009; 84(3): 296–302CrossRefPubMedGoogle Scholar
  56. 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): 1086–1093CrossRefPubMedGoogle Scholar
  57. 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): 51–60CrossRefPubMedGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Palka Kaur Khanuja
    • 1
    Email author
  • Satish Chander Narula
    • 1
  • Rajesh Rajput
    • 2
  • Rajinder Kumar Sharma
    • 1
  • Shikha Tewari
    • 1
  1. 1.Department of Periodontics and Oral ImplantologyPGIDS Post Graduate Institute of Dental SciencesRohtakIndia
  2. 2.Department of Medicine Unit VII and EndocrinologyPGIMS Post Graduate Institute of Medical SciencesRohtakIndia

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