Journal of Peking University(Health Sciences) ›› 2020, Vol. 52 ›› Issue (1): 71-76. doi: 10.19723/j.issn.1671-167X.2020.01.011

Previous Articles     Next Articles

Associations of impaired glucose metabolism with chronic peridontitis in pre-diabetes patients

Yong ZHANG(),Chang LIU2,Bin CHEN3,Fan CHEN4,Jin-yu DUAN1,Meng-jun ZHANG1,Jian JIAO1   

  1. 1. First Clinical Division, Peking University School and Hospital of Stomatology & National Clinical Research Center for Oral Diseases & National Engineering Laboratory for Digital and Material Technology of Stomatology & Beijing Key Laboratory of Digital Stomatology, Beijing 100081, China
    2. Department of Oncology, the Seventh Medical Center of PLA General Hospital, Beijing 100700, China
    3. Department of Endocrinology and Metabolism, the Seventh Medical Center of PLA General Hospital, Beijing 100700, China
    4. Department of Stomatology, Peking University People’s Hospital, Beijing 100044, China
  • Received:2018-10-07 Online:2020-02-18 Published:2020-02-20
  • Contact: Yong ZHANG E-mail:zhangyong_1019@163.com
  • Supported by:
    Supported by the National Natural Science Foundation of China(81800978)

Abstract:

Objective: To investigate the associations of impaired glucose metabolism and insulin resis-tance with chronic periodontitis in pre-diabetes patients. Methods: A cross-sectional analysis was conducted and we included a total of 171 pre-diabetes patients aged 30-65 years, free of diabetes. Pre-diabetes was defined as impaired fasting glucose (IFG) [fasting glucose (FG): 6.1-7.0 mmol/L] and/or impaired glucose tolerance (IGT) [oral glucose tolerance test (OGTT): 7.8-11.0 mmol/L]. Chronic periodontitis was defined according to Centers for Disease Control and Prevention (CDC)/American Academy of Periodontology (AAP) definition and the patients were divided into mild, moderate, and severe chronic periodontitis groups [mild: at least two interproximal sites with clinical attachment loss (CAL) ≥3 mm and at least two interproxima sites with probing depth (PD) ≥4 mm or 1 site with PD≥5 mm; moderate: at least two interproximal sites with CAL ≥4 mm and at least two interproxima sites with at least two interproximal sites with PD ≥5 mm; severe: at least two interproximal sites with CAL ≥6 mm and at least one interproxima site with at least two interproximal sites with PD≥5 mm]. A periodontal examination indexes [plaque index (PLI), PD, CAL, and bleeding on probing (BOP)] and glucose metabolism indexes [FG, OGTT, hemoglobinA1c (HbA1c), fasting insulin and homeostasis model assessments of insulin resistance (HOMA-IR)] were measured. The association of glucose meta-bolism and chronic periodontitis was investigated by multivariable logistic regression analysis. Results: FG in the moderate and severe chronic periodontitis groups was significantly higher compared with mild chronic periodontitis group, HOMA-IR in the moderate and severe chronic periodontitis groups was signi-ficantly higher compared with mild chronic periodontitis group, OGTT in the severe chronic periodntitis group was significantly higher compared with mild chronic peridontitis group and moderate chronic pe-riodontitis groups, and there was no significant difference between moderate and mild chronic periodontitis groups. For the insulin and HbA1c, there was no significant difference among mild, moderate and severe chronic periodontitis groups. After multivariable adjustment of age, gender, smoking status, hypertension and body mass index, IFG (OR=1.39, 95%CI: 1.01-1.98) and HOMA-IR (OR=1.36, 95%CI: 1.04-1.76) were associated with moderate periodontitis; IFG (OR=1.64, 95%CI: 1.17-2.40), IGT (OR=1.65, 95%CI: 1.21-2.26), and HOMA-IR (OR=1.72, 95%CI: 1.23-2.41) were significantly associated with severe periodontitis. Conclusion: Our data provided evidences that impaired glucose metabolism were associated with chronic periodontitis among pre-diabetes patients.

Key words: Pre-diabetes, Chronic periodontitis, Impaired glucose metabolism, Insulin resistance

CLC Number: 

  • R781.4

Table 1

Characteristics of glucose metabolism in three periodontitis patient groups"

Glucose metabolism Mild chronic periodontitis (n=74) Moderate chronic periodontitis (n=55) Severe chronic periodontitis (n=42)
IFG 13 (18%) 7 (13%) 2 (5%)
IGT 46 (62%) 26 (47%) 10 (24%)
IFG+IGT 15 (20%) 22 (40%)* 30 (71%)*#

Table 2

Characteristics of general condition, periodontal status and glucose metabolism of patients in each group"

Items Mild chronic periodontitis (n=74) Moderate chronic periodontitis (n=55) Severe chronic periodontitis (n=42)
Age/years, x?±s 49.54±6.76 51.92±6.61 51.72±6.80
Gender (Male/Female), n 32/42 23/32 24/18
Smoking 11 (15%) 8 (15%) 7 (17%)
Hypertension 42 (57%) 30 (55%) 24 (57%)
BMI, x?±s 22.34±4.65 22.68±4.52 23.27±3.61
Number of lost tooth, x?±s 0.63±1.35 1.82±1.28* 2.50±1.20*
PLI, x?±s 0.63±0.54 0.91±0.61* 1.38±0.65*#
PD/mm, x?±s 2.42±0.15 3.31±0.21* 3.64±0.72*#
CAL/mm, x?±s 1.09±0.51 2.22±0.71* 2.83±1.23*#
BOP/%, x?±s 11±14 20±17* 44±26*#
FG/(mmol/L), x?±s 5.89±0.44 6.22±0.43* 6.61±0.50*#
OGTT/(mmol/L), x?±s 8.13±0.65 8.32±0.91 8.95±0.67*#
HbA1c/%, x?±s 5.55±0.52 5.57±0.51 5.65±0.47
Fasting insulin/(mIU/L), x?±s 10.47±7.51 10.41±5.43 10.37±7.50
HOMA-IR, x?±s 2.47±0.87 2.59±1.37* 2.74±1.72*#

Table 3

Binary Logistic regressions of glucose metabolism levels and periodontitis status in pre-diabetes patients*"

Items Mild chronic periodontitis (n=74) Moderate-severe chronic periodontitis (n=97)
OR 95%CI P value
Fasting glucose 1 1.53 1.13-2.10 0.003
OGGT 1 1.35 1.04-1.75 0.018
HbA1c 1 1.17 0.88-1.55 0.828
Fasting insulin 1 0.95 0.90-1.00 0.056
HOMA-IR 1 1.57 1.17-2.10 0.004

Table 4

Multinomial Logistic regressions of glucose metabolism levels and periodontitis status in pre-diabetes patients*"

Items Mild chronic periodontitis (n=74) Moderate chronic periodontitis (n=55) Severe chronic periodontitis (n=42)
OR 95%CI P value OR 95%CI P value
Fasting glucose 1 1.39 1.01-1.98 0.003 1.64 1.17-2.40 0.003
OGGT 1 1.16 0.87-1.56 0.307 1.65 1.21-2.26 0.002
HbA1c 1 1.15 0.87-1.48 0.832 1.20 0.95-1.61 0.804
Fasting insulin 1 0.94 0.90-1.02 0.173 0.96 0.88-1.00 0.067
HOMA-IR 1 1.36 1.04-1.76 0.009 1.72 1.23-2.41 0.002
[1] 孟焕新 . 牙周炎与糖尿病的关系[J]. 北京大学学报(医学版), 2007,39(1):18-20.
[2] 和璐, 廖雁婷 . 牙周炎与2型糖尿病[J]. 中国糖尿病杂志, 2010,2(4):242-245.
[3] Lalla E, Papapanou PN . Diabetes mellitus and periodontitis: a tale of two common interrelated diseases[J]. Nat Rev Endocrinol, 2011,7(12):738-748.
[4] Jepsen S, Stadlinger B, Terheyden H , et al. Science transfer: oral health and general health—the links between periodontitis, atherosclerosis and diabetes[J]. J Clin Periodontol, 2016,42(12):1071-1073.
[5] Schallhorn RA . Understanding the inter-relationship between pe-riodontitis and diabetes: Current evidence and clinical implications[J]. Compend Contin Educ Dent, 2016,37(6):368-370.
[6] Yang W, Lu J, Weng J , et al. Prevalence of diabetes among men and women in China[J]. N Engl J Med, 2010,362(25):1090-1101.
[7] 中华医学会糖尿病学分会. 中国2型糖尿病防治指南(2013年版)[J]. 中华内分泌代谢杂志, 2014,30(10):893-942.
[8] Tabak AG, Herder C, Rathmann W , et al. Prediabetes: a high-risk state for diabetes development[J]. Lancet, 2012,379(9833):2279-2290.
[9] Demmer RT, Desvarieux M, Holtfreter B , et al. Periodontal status and hemoglobin A1C change: Longitudinal results from the study of health in Pomerania (SHIP)[J]. Diabetes Care, 2010,33(5):1037-1043.
[10] Chiu SY, Lai H, Yen AM , et al. Temporal sequence of the bidirectional relationship between hyperglycemia and periodontal disease: a community-based study of 5,885 Taiwanese aged 35-44 years (KCIS No. 32)[J]. Acta Diabetol, 2015,52(1):123-131.
[11] Saito T, Shimazaki Y, Kiyohara Y , et al. Relationship between obesity, glucose tolerance, and periodontal disease in Japanese women: the Hisayama study[J]. J Periodontal Res, 2005,40(4):346-353.
[12] Arora N, Papapanou PN, Rosenbaum M , et al. Periodontal infection, impaired fasting glucose and impaired glucose tolerance: results from the Continuous National Health and Nutrition Examination Survey 2009-2010[J]. J Clin Periodontol, 2014,41(7):643-652.
[13] Kowall B, Holtfreter B, Völzke H , et al. Pre-diabetes and well-controlled diabetes are not associated with periodontal disease: the SHIP Trend Study[J]. J Clin Periodontol, 2015,42(5):422-430.
[14] 黄艳丽, 郭维华, 田卫东 . 糖尿病前期和牙周炎的相互关系[J]. 国际口腔医学杂志, 2016,43(6):706-710.
[15] Page RC, Eke PI . Case definitions for use in population-based surveillance of periodontitis[J]. J Periodontol, 2007,78(7 Suppl):1387-1399.
[16] Hong M, Yeon KH, Hannah S , et al. Prevalence and risk factors of periodontitis among adults with or without diabetes mellitus[J]. Korean J Intern Med, 2016,31(5):910-919.
[17] Javed F, Thafeed Alghamdi AS, Mikami T , et al. Effect of glycemic control on self-perceived oral health, periodontal parameters, and alveolar bone loss among patients with prediabetes[J]. J Periodontol, 2014,85(2):234-241.
[18] Choi YH, Mckeown RE, Mayer-Davis EJ , et al. Association between periodontitis and impaired fasting glucose and diabetes[J]. Diabetes Care, 2011,34(2):381-386.
[19] Pérez CM, Muñoz F, Andriankaja OM , et al. Cross-sectional associations of impaired glucose metabolism measures with bleeding on probing and periodontitis[J]. J Clin Periodontol, 2017,44(2):142-149.
[20] Benguigui C, Bongard V, Ruidavets JB , et al. Metabolic syndrome, insulin resistance, and periodontitis: a cross-sectional study in a middle-aged French population[J]. J Clin Periodontol, 2010,37(7):601-608.
[21] Lim SG, Han K, Kim HA , et al. Association between insulin resistance and periodontitis in Korean adults[J]. J Clin Periodontol, 2014,41(2):121-130.
[22] Timonen P, Saxlin T, Knuuttila M , et al. Role of insulin sensiti-vity and beta cell function in the development of periodontal disease in adults without diabetes[J]. J Clin Periodontol, 2013,40(12):1079-1086.
[23] Timonen P, Suominen-Taipale L, Jula A , et al. Insulin sensitivity and periodontal infection in a non-diabetic, non-smoking adult population[J]. J Clin Periodontol, 2011,38(1):17-24.
[24] American Diabetes Association . Diagnosis and classification of diabetes mellitus. Clinical practice recommendations 2004[J]. Diabetes Care, 2010,37(Suppl 1):S81-S90.
[25] Islam SK, Seo M, Lee YS , et al. Association of periodontitis with insulin resistance, β-cell function, and impaired fasting glucose before onset of diabetes[J]. Endocr J, 2015,62(11):981-989.
[26] Demmer RT, Jacobs DR Jr, Singh R , et al. Periodontal bacteria and prediabetes prevalence in ORIGINS: The Oral Infections, Glucose Intolerance, and Insulin Resistance Study[J]. J Dent Res, 2015,94(9 Suppl):201S-211S.
[27] Demmer RT, Squillaro A, Papapanou PN , et al. Periodontal infection, systemic inflammation, and insulin resistance: results from the continuous National Health and Nutrition Examination Survey (NHANES) 1999-2004[J]. Diabetes Care, 2012,35(11):2235-2242.
[1] Xiao-yuan ZHANG,Cheng-cheng GUO,Ying-xiang YU,Lan XIE,Cui-qing CHANG. Establishment of high-fat diet-induced obesity and insulin resistance model in rats [J]. Journal of Peking University (Health Sciences), 2020, 52(3): 557-563.
[2] Shu-wen SHI,Yang MENG,Jian JIAO,Wen-jing LI,Huan-xin MENG,Qing-xian LUAN,Wan-chun WANG. Tooth loss and multivariable analysis after 5-year non-surgical periodontal treatment on molars with furcation involvement [J]. Journal of Peking University(Health Sciences), 2019, 51(5): 913-918.
[3] ZHANG You-wen, XIN Tian-yi, JIAO Jian,ZHOU Yan-heng, SHI Jie. Extraction-orthodontic treatment on patients with chronicperiodontitis: a preliminary study [J]. Journal of Peking University(Health Sciences), 2018, 50(2): 308-313.
[4] ZHANG Jin, XING Yan, WANG Xin-Li, GUAN Yu-Hong, ZHANG Hui. Decreased insulin sensitivity in rat hepatocytes with intrauterine growth retardation and establishment of insulin resistance cell model in vitro [J]. Journal of Peking University(Health Sciences), 2014, 46(3): 464-468.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] . [J]. Journal of Peking University(Health Sciences), 2009, 41(4): 456 -458 .
[2] . [J]. Journal of Peking University(Health Sciences), 2009, 41(2): 125 -128 .
[3] . [J]. Journal of Peking University(Health Sciences), 2009, 41(2): 135 -140 .
[4] . [J]. Journal of Peking University(Health Sciences), 2009, 41(2): 158 -161 .
[5] . [J]. Journal of Peking University(Health Sciences), 2009, 41(2): 217 -220 .
[6] . [J]. Journal of Peking University(Health Sciences), 2009, 41(1): 52 -55 .
[7] . [J]. Journal of Peking University(Health Sciences), 2009, 41(1): 109 -111 .
[8] . [J]. Journal of Peking University(Health Sciences), 2009, 41(3): 297 -301 .
[9] . [J]. Journal of Peking University(Health Sciences), 2009, 41(5): 599 -601 .
[10] . [J]. Journal of Peking University(Health Sciences), 2009, 41(5): 516 -520 .