1. Department of Periodontics and Oral Implantology; PGIDS Post Graduate Institute of Dental Sciences, Rohtak, Haryana 124001, India
2. Department of Medicine Unit VII and Endocrinology; PGIMS Post Graduate Institute of Medical Sciences, Rohtak, Haryana 124001, India
Khanuja.palka@gmail.com
Show less
History+
Received
Accepted
Published Online
2015-09-22
2016-08-17
2016-12-01
PDF
(258KB)
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 (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.
Palka Kaur Khanuja, Satish Chander Narula, Rajesh Rajput, Rajinder Kumar Sharma, Shikha Tewari.
Association of periodontal disease with glycemic control in patients with type 2 diabetes in Indian population.
Front. Med., 2017, 11 (1) : 110-119 DOI:10.1007/s11684-016-0484-5
TaylorJJ, PreshawPM, LallaE. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol2013; 40(Suppl 14): S113–S134
[2]
KingGL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol2008; 79(8Suppl ): 1527–1534
[3]
GravesDT, KayalRA. Diabetic complications and dysregulated innate immunity. Front Biosci2008; 13(13): 1227–1239
LöeH. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care1993; 16(1): 329–334
[6]
GarciaRI, HenshawMM, KrallEA. Relationship between periodontal disease and systemic health. Periodontol 20002001; 25(1): 21–36
[7]
AmarS, HanX. The impact of periodontal infection on systemic diseases. Med Sci Monit2003; 9(12): RA291–RA299
[8]
LuHK, YangPC. Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent2004; 24(1): 71–79
[9]
CampusG, SalemA, UzzauS, BaldoniE, TonoloG. Diabetes and periodontal disease: a case-control study. J Periodontol2005; 76(3): 418–425
[10]
LuHK, YangPC. Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent2004; 24(1): 71–79
[11]
NovakKF, TaylorGW, DawsonDR, FergusonJE 2nd, NovakMJ. Periodontitis and gestational diabetes mellitus: exploring the link in NHANES III. J Public Health Dent2006; 66(3): 163–168
[12]
NovakMJ, PotterRM, BlodgettJ, EbersoleJL. Periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol2008; 79(4): 629–636
[13]
WangTT, ChenTH, WangPE, LaiH, LoMT, ChenPY, ChiuSY. 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 Periodontol2009; 36(5): 372–379
[14]
RajhansNS, KohadRM, ChaudhariVG, MhaskeNH. A clinical study of the relationship between diabetes mellitus and periodontal disease. J Indian Soc Periodontol2011; 15(4): 388–392
[15]
PathakAK, ShakyaVK, ChandraA, GoelK. Association between diabetes mellitus and periodontal status in north Indian adults. European J Gen Dent2013; 2(1): 58–61
[16]
KalraN, PradeepAR, PriyankaN, KumariM. 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 Sci2013; 55(1): 57–62
[17]
TandonV, TangadeP, LingeshaRT, TirthA, PalSK, YadavV. Glycemic control and periodontal disease in type 2 diabetes mellitus patients: a cross-sectional study. J Indian Assoc Public Health Dent2015; 13(3): 297–301
[18]
TaylorGW, BurtBA, BeckerMP, GencoRJ, ShlossmanM, KnowlerWC, PettittDJ. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol1996; 67(10 Suppl): 1085–1093
TaylorGW, BorgnakkeWS. Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis2008; 14(3): 191–203
[21]
NesseW, LindeA, AbbasF, SpijkervetFK, DijkstraPU, de BrabanderEC, GerstenbluthI, VissinkA. Dose-response relationship between periodontal inflamed surface area and HbA1c in type 2 diabetics. J Clin Periodontol2009; 36(4): 295–300
[22]
AbraoL, ChagasJK, SchmidH. Periodontal disease and risk for neuropathic foot ulceration in type 2 diabetes. Diabetes Res Clin Pract2010; 90(1): 34–39
[23]
ChenL, WeiB, LiJ, LiuF, XuanD, XieB, ZhangJ. Association of periodontal parameters with metabolic level and systemic inflammatory markers in patients with type 2 diabetes. J Periodontol2010; 81(3): 364–371
[24]
MoritaT, YamazakiY, MitaA, TakadaK, SetoM, NishinoueN, SasakiY, MotohashiM, MaenoM. A cohort study on the association between periodontal disease and the development of metabolic syndrome. J Periodontol2010; 81(4): 512–519
[25]
DemmerRT, DesvarieuxM, HoltfreterB, JacobsDR Jr, WallaschofskiH, NauckM, VölzkeH, KocherT. Periodontal status and A1C change: longitudinal results from the study of health in Pomerania (SHIP). Diabetes Care2010; 33(5): 1037–1043
[26]
SusantoH, NesseW, DijkstraPU, HoedemakerE, van ReenenYH, AgustinaD, VissinkA, AbbasF. Periodontal inflamed surface area and C-reactive protein as predictors of HbA1c: a study in Indonesia. Clin Oral Investig2012; 16(4): 1237–1242
[27]
SoutherlandJH, MossK, TaylorGW, BeckJD, PankowJ, GangulaPR, OffenbacherS. Periodontitis and diabetes associations with measures of atherosclerosis and CHD. Atherosclerosis2012; 222(1): 196–201
[28]
KimEK, LeeSG, ChoiYH, WonKC, MoonJS, MerchantAT, LeeHK. Association between diabetes-related factors and clinical periodontal parameters in type-2 diabetes mellitus. BMC Oral Health2013; 13: 64PMID:24195646
[29]
CasanovaL, HughesFJ, PreshawPM. Diabetes and periodontal disease: a two-way relationship. Br Dent J2014; 217(8): 433–437
[30]
AmiriAA, MaboudiA, BaharA, FarokhfarA, DaneshvarF, KhoshgoeianHR, NasohiM, KhalilianA. Relationship between type 2 diabetic retinopathy and periodontal disease in Iranian adults. N Am J Med Sci2014; 6(3): 139–144
[31]
GokhaleNH, AcharyaAB, PatilVS, TrivediDJ, SettyS, ThakurSL. Resistin levels in gingival crevicular fluid of patients with chronic periodontitis and type 2 diabetes mellitus. J Periodontol2014; 85(4): 610–617
[32]
SimpsonTC, WeldonJC, WorthingtonHV, NeedlemanI, WildSH, MolesDR, StevensonB, FurnessS, Iheozor-EjioforZ. Treatment of periodontal disease for glycaemic control in people with diabetes mellitus. Cochrane Database Syst Rev2015; 11(11): CD004714
[33]
TeeuwWJ, GerdesVE, LoosBG. Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and meta-analysis. Diabetes Care2010; 33(2): 421–427
[34]
LiewAK, PunnanithinontN, LeeYC, YangJ. Effect of non-surgical periodontal treatment on HbA1c: a meta-analysis of randomized controlled trials. Aust Dent J2013; 58(3): 350–357
[35]
EngebretsonS, KocherT. Evidence that periodontal treatment improves diabetes outcomes: a systematic review and meta-analysis. J Periodontol2013; 84(4 Suppl): S153–S169
[36]
SgolastraF, SeverinoM, PietropaoliD, GattoR, MonacoA. 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 Periodontol2013; 84(7): 958–973
[37]
MohanM, JhingranR, BainsVK, GuptaV, MadanR, RizviI, ManiK. 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 Sci2014; 44(4): 158–168
[38]
BhopalR, RankinJ. Concepts and terminology in ethnicity, race and health: be aware of the ongoing debate. Br Dent J1999; 186(10): 483–484
[39]
PageRC, EkePI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol2007; 78(7 Suppl): 1387–1399
[40]
CostaFO, GuimarãesAN, CotaLO, PataroAL, SegundoTK, CortelliSC, CostaJE. Impact of different periodontitis case definitions on periodontal research. J Oral Sci2009; 51(2): 199–206
[41]
ManauC, EcheverriaA, AguedaA, GuerreroA, EcheverriaJJ. Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. J Clin Periodontol2008; 35(5): 385–397
[42]
NesseW, AbbasF, van der PloegI, SpijkervetFKL, DijkstraPU, VissinkA. Periodontal inflamed surface area: quantifying inflammatory burden. J Clin Periodontol2008; 35(8): 668–673
[43]
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care2010; 33(Suppl 1): S62–S69
[44]
SilnessJ, LoeH. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand1964; 22(1): 121–135
[45]
LöeH, SilnessJ. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand1963; 21(6): 533–551
[46]
GencoRJ. Current view of risk factors for periodontal diseases. J Periodontol1996; 67(10 Suppl): 1041–1049
ChoiBC, ShiF. Risk factors for diabetes mellitus by age and sex: results of the National Population Health Survey. Diabetologia2001; 44(10): 1221–1231
[49]
ImreyPB. Considerations in the statistical analysis of clinical trials in periodontitis. J Clin Periodontol1986; 13(5): 517–528
[50]
WolffRE, WolffLF, MichalowiczBS. A pilot study of glycosylated hemoglobin levels in periodontitis cases and healthy controls. J Periodontol2009; 80(7): 1057–1061
[51]
NibaliL, D’AiutoF, GriffithsG, PatelK, SuvanJ, TonettiMS. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case-control study. J Clin Periodontol2007; 34(11): 931–937
[52]
KolbH, Mandrup-PoulsenT. The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation. Diabetologia2010; 53(1): 10–20
[53]
EngebretsonS, ChertogR, NicholsA, Hey-HadaviJ, CelentiR, GrbicJ. Plasma levels of tumour necrosis factor-α in patients with chronic periodontitis and type 2 diabetes. J Clin Periodontol2007; 34(1): 18–24
[54]
ParaskevasS, HuizingaJD, LoosBG. A systematic review and meta-analyses on C-reactive protein in relation to periodontitis. J Clin Periodontol2008; 35(4): 277–290
[55]
EbrahimiA, NabipourI, VahdatK, JafariSM, FouladvandM, AssadiM, MovahedA, ObeidiN, SanjdidehZ. High sensitivity C-reactive protein is associated with the metabolic syndrome independent to viral and bacterial pathogen burden. Diabetes Res Clin Pract2009; 84(3): 296–302
[56]
HungCH, LeeCM, ChenCH, HuTH, JiangSR, WangJH, LuSN, WangPW. Association of inflammatory and anti-inflammatory cytokines with insulin resistance in chronic hepatitis C. Liver Int2009; 29(7): 1086–1093
[57]
HujoelPP, DrangsholtM, SpiekermanC, DeRouenTA. Periodontitis-systemic disease associations in the presence of smoking—causal or coincidental? Periodontol 20002002; 30(1): 51–60
RIGHTS & PERMISSIONS
Higher Education Press and Springer-Verlag Berlin Heidelberg