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Table 2 Summary of results of cohort studies

From: Epidemiologic relationship between periodontitis and type 2 diabetes mellitus

Study

Characteristics

Definition of outcome

Definition of exposure

Main conclusion and outcome

T2DM/non-T2DM

Chiu

2015 [62]

Taiwan,

KCIS study

5y FU (2003–2008)

Binary variable

PD: CPI ≥ 3

Non-PD: CPI < 3

T2DM: FBG ≥ 126 mg/dl or self-reported T2DM (N = 57)

Pre-diabetes: 100 ≤ FBG < 126 mg/dl (N = 297)

None: FBG < 100 mg/dl (N = 4033)

T2DM led to a 95% elevated risk for incident PD. Adjusted HR = 1.95, 95%CI 1.22–3.13

Pre-diabetes led to a 25% elevated risk for incident PD. Adjusted HR = 1.25, 95%CI 1.00–1.57

Demmer 2012 [23]

Germany,

SHIP study

5y FU

(1997–2006)

Binary variable

Tooth loss or not

T2DM: Self-reported age > 30 years old, or HbA1c ≥ 6.5%, timing of insulin therapy initiation > 1 year from diagnosis

Controlled T2DM: HbA1c ≤ 7% (N = 80)

Uncontrolled T2DM: HbA1c > 7% (N = 72)

Control: no DM (N = 2280)

Controlled T2DM did not lead to an elevated risk for tooth loss.

Adjusted RR = 1.01, 95%CI 0.79–1.28

Uncontrolled T2DM led to a 36% elevated risk for tooth loss. Adjusted RR = 1.36, 95%CI 1.11–1.67

Continuous variable

Mean PPD change;

Mean CAL change;

Controlled T2DM did not lead to an increased PPD and CAL change. Adjusted MD = 0.04 and 0.09 mm, p > 0.05

Uncontrolled T2DM led to a significant increase in PPD and CAL change. Adjusted MD = 0.18 and 0.37 mm, p < 0.05

Jimenez 2012 [65]

USA,

HPFS study,

20y FU (1986-NA)

Binary variable

PD: self-reported;

Tooth loss: self-reported

T2DM: self-reported T2DM (N = 2285)

Control: non-T2DM (N = 32,962)

T2DM led to a 29% elevated risk for incident PD. Adjusted RR = 1.29, 95%CI 1.13–1.47

T2DM led to a 9% elevated risk for incident tooth loss. Adjusted RR = 1.09, 95%CI 1.01–1.18

Morita 2012 [68]

Japan,

5y FU (1997–2006)

Binary variable

PD: CPI ≥ 3

Non-PD: CPI < 3

T2DM: HbA1c ≥ 6.5% (N = 150)

Control: HbA1c < 6.5% (N = 5706)

T2DM led to a 17% elevated risk for incident PD. Adjusted RR = 1.17, 95%CI 1.01–1.36

Nelson 1990 [39]

USA,

Pima Indians study,

Mean 2.6y FU

(1983–1989)

Binary variable

PD: < 24 teeth present;>  6 teeth with ≥25% bone loss and any tooth with ≥50% bone loss.

Non-PD: ≥24 teeth present; < 6 could have 25–50% bone loss and the rest < 25% bone loss

T2DM: OGTT ≥11.1 mM(N = 56)

Control: no T2DM (N = 645)

T2DM led to a 160% elevated risk for incident PD. Adjusted RR = 2.57, 95%CI 1.0–6.6, p < 0.05

Taylor

1998 [69]

USA, Pima Indians study,

Mean 2.3y FU

(1.2–6.9 years)

Mean alveolar bone loss

bone scores corresponded to bone loss of 0, 1to 24%, 25 to 49%, 50 to 74%, or > 75%

Diagnosed by OGTT (> 200 mg/dl)

Better controlled T2DM: HbA1c ≤ 9% (N = 7)

Poorer controlled T2DM: HbA1c > 9% (N = 14)

Control: no T2DM (N = 338)

Better controlled T2DM led to a 120% elevated risk for alveolar bone loss progression, but was not statistically significant. Adjusted OR = 2.2, 95%CI 0.7–6.5, p = 0.175

Poorer controlled T2DM led to a 1040% elevated risk for alveolar bone loss progression. Adjusted OR = 11.4, 95%CI 2.5–53.3

PD/non-PD

Demmer 2008 [63]

USA,

NHEFS study

17y FU

(1971–1992)

T2DM:

Death certificate; self-reported T2DM and received anti-diabetes medications; facility discharge diagnosis

Category of baseline periodontal index, control group was the participants with lowest RPI score

Compared to the control group, participants in the 1st or 2nd categories did not experience an increased OR of developing T2DM, whereas the odds increased sharply in the 3rd category (OR 2.08; P < 0.0001). The ORs in 4th (1.71; P = 0.003) and 5th (1.50; P = 0.06) categories abated but remained elevated and were not statistically significantly different from the odds for those in the 3rd category.

PD: clinical diagnosed(N = 1662)

Gingivitis: clinical diagnosed (N = 2135)

Control: periodontium health (N = 3372)

PD led to a 50% elevated risk for incident T2DM.

Adjusted OR≈1.50, 95%CI NA, p < 0.05

Gingivitis led to a 40% elevated risk for incident T2DM.

Adjusted OR≈1.40, 95%CI NA, p < 0.05

Exposure: LOT 25–31 (N=NA)

Control: LOT 0–8 (N=NA)

Loss more teeth at baseline led to a 70% elevated risk for incident T2DM. Adjusted OR≈1.70, 95%CI NA, p < 0.05

Ide

2010 [64]

Japan,

6.3y FU

(2000–2007)

T2DM:

FBG ≥ 125 mg/dl

Exposure1: CPI = 4 (N = 490)

Exposure2: CPI = 3 (N = 2167)

Control: CPI < 3 (N = 3191)

CPI = 4 led to a 28% elevated risk for incident T2DM, but was not statistically significant.

Adjusted HR = 1.28, 95%CI 0.89–1.86

CPI = 3 did not led to an elevated risk for incident T2DM.

Adjusted HR = 1.00, 95%CI 0.77–1.30

Exposure1: LOT> 3 (N = 748)

Exposure2: 1 < LOT< 3 (N = 2265)

Control: LOT = 0 (N = 2835)

Loss more than 3 teeth did not lead to an elevated risk for incident T2DM

Adjusted HR = 0.98 95%CI 0.69–1.39

Loss 1 or 2 teeth did not lead to an elevated risk for incident T2DM. Adjusted HR = 1.02 95%CI 0.79–1.32

Kebede

2017 [66]

Germany,

SHIP study

11.1y FU

(1997–2012)

T2DM:

Self-reported physician diagnosed T2DM or treatment with antidiabetic medication

Exposure: mean PPD 2.70–7.25 mm (N=NA)

Control: mean PPD 0.95–1.97 mm (N=NA)

Deeper PPD did not lead to an elevated risk for incident T2DM.

Adjusted incidence RR = 1.271 95% 0.782–2.065

Exposure: mean CAL 3.15–12.25 mm (N=NA)

Control: mean CAL 0–1.15 mm (N=NA)

Higher CAL did not lead to an elevated risk for incident T2DM.

Adjusted incidence RR = 0.819 95%CI 0.489–1.370

Miyawaki 2016 [67]

Japan,

My health up Study,

all male

5y FU

(2004–2009)

T2DM: self-reported T2DM and received anti-diabetes medications, or based on clinical test (FBG ≥ 126 mg/dl or HbA1C ≥ 6.5%)

Exposure: self-reported tooth loosening (N = 262)

Control: without tooth loosening (N = 2207)

Tooth loosening led to a 73% elevated risk for incident T2DM.

Adjusted RR = 1.73, 95%CI 1.18–2.53

Exposure: self-reported gingival bleeding (N = 795)

Control: without gingival bleeding (N = 1674)

Gingival bleeding led to a 23% elevated risk for incident T2DM, but was not statistically significant.

Adjusted RR = 1.23, 95%CI 0.90–1.70

Morita 2012 [68]

Japan,

5y FU

(1997–2006)

T2DM: HbA1c ≥ 6.5%

Exposure1: CPI = 4 (N = 1634)

Exposure2: CPI = 3 (N = 4114)

Control: CPI = 0 (N = 1647)

CPI = 4 led to a 245% elevated risk for incident T2DM.

Adjusted RR = 3.45, 95%CI 1.08–11.02, p = 0.037

CPI = 3 led to a 145% elevated risk for incident T2DM, but was not statistically significant.

Adjusted RR = 2.47, 95%CI 0.78–7.79, p = 0.122

Myllymki 2018 [70]

Finland, Cohort 1935 Survey,

15-18y FU

(1990–2008)

T2DM: WHO 1995 criteria

Exposure1: PPD = 4-5 mm (N = 98)

Exposure2: PPD > 6 mm (N = 91)

Control: No deep pockets (N = 88)

Both two exposures did not increase the T2DM incidence.

4-5 mm PPD: adjusted RR = 1.32, 95%CI 0.69–2.53, p > 0.05

> 6 mm PPD: adjusted RR = 1.56, 95%CI 0.84–2.92, p > 0.05

Winning 2016 [71]

UK,

PRIME study

7.8y FU

(2001–2010)

T2DM: FBG ≥ 126 mg/dl and WHO criteria

Exposure1: moderate PD

Exposure2: severe PD

Moderate/severe PD total = 553

Control: No significant PD (N = 778)

PD severity was based on CDC/AAP classification

Moderate PD led to a 53% elevated risk for developing T2DM, but was not statistically significant.

Adjusted RR = 1.53, 95%CI 0.86–2.74, p > 0.05

Severe PD led to an 85% elevated risk for developing T2DM

Adjusted RR = 1.85, 95%CI 1.06–3.22, p < 0.05

  1. PD: periodontitis; T2DM: type 2 diabetes mellitus; CAL: clinical attachment loss; PPD: periodontal pocket depth; LOT: loss of teeth; OGTT: oral glucose tolerance test; HbA1c: glycated hemoglobin; FBG: fasting plasma glucose; CI: confidence intervals; OR: odds ratio; RR: risk ratios; HR: hazard ratio; CPI: community periodontal index; RPI: Russell periodontal index