Periodontal disease is associated with increased coronary heart disease risk: A meta-analysis based on 38 case-control studies

Table 1 Characteristics and methodological quality of included 38 case-control studies in the meta-analysis

Ref.	Location	Sample size	Age (case/control, yr)	Source of control	Assessment		End points	OR (95%CI)	NOS
					PD	CHD
Li et al[13]	China	88/128	> 60	Hospital-based	PI	C	CHD	1.85 (1.07-3.20)	4
López et al[14]	Chile	35/51	42.5 ± 5.7/40.5 ± 6.3	Hospital-based	PPD	ECG	CHD	3.17 (1.31-7.65)1	6
Huang et al[15]	China	146/136	58.7 ± 8.9	Hospital-based	Q	CAG	CHD	2.27 (1.40-3.68)	5
Liu et al[16]	China	216/216	59.4 ± 15.3/57.9 ± 13.7	Population-based	PI	CAG	CHD	5.42 (3.32-8.86)	4
Rutger Persson et al[17]	Sweden	80/80	63.4 ± 8.9/61.9 ± 9.1	Population-based	ABL	ECG	MI	14.1 (5.8-34.4)1	7
Geerts et al[18]	Belgium	108/62	59.2 ± 10.9/57.7 ± 8.7	Hospital-based	PPD	C	CHD	6.50 (1.80-23)1	7
Montebugnoli et al[19]	Italy	63/50	52.3 ± 4.9/54.5 ± 6.1	Population-based	PPD	CAG	CHD	4.61 (1.00-23.20)1	8
Renvert et al[20]	Sweden	88/80	62.7 ± 9.1/NA	Hospital-based	PPD	C	MI	7.67 (1.13-51.92)1	6
Tang et al[21]	China	250/250	≥ 45	Hospital-based	CPI	C	CHD	1.95 (1.36-2.78)	4
Buhlin et al[22]	Sweden	143/50	65.9 ± 8.6/64.5 ± 8.3	Population-based	PPD	CAG	CHD	3.80 (1.68-8.74)1	8
Liu et al[23]	China	45/40	54.9 ± 8.1/51.2 ± 6.5	Hospital-based	PI	CAG	CHD	18.70 (6.25-55.93)	4
Wang et al[24]	China	216/216	59 ± 15/58 ± 14	Population-based	ABL	CAG	CHD	1.76 (1.31-2.36)1	7
Andriankaja et al[25]	United States	537/800	54.6 ± 8.5/55.0 ± 0.0	Population-based	CAL	C	MI	2.24 (1.60-3.13)1	8
Barilli et al[26]	Brazil	40/59	49.2 (30-79)	Hospital-based	CPI	C	CHD	61 (17.26-214.86)	5
Briggs et al[27]	United Kingdom	92/79	56.7 ± 6.3/58.2 ± 6.7	Population-based	PPD	CAG	CHD	3.06 (1.02-9.17)1	8
Geismar et al[28]	Denmark	110/140	65/62.6	Hospital-based	ABL	ECG	CHD	2.0 (0.77-5.08)1	7
Li et al[29]	China	357/305	72.5 ± 8.9	Population-based	PI	CAG	CHD	1.16 (0.91-1.48)	6
Spahr et al[30]	Germany	263/526	61.0 ± 7.1/61.0 ± 7.1	Population-based	CPI	CAG	CHD	1.67 (1.08-2.58)1	8
Zhang et al[31]	China	77/74	50.2 ± 9.6/50.8 ± 9.5	Population-based	PPD	CAG	CHD	2.13 (1.08-4.22)	6
Zhang et al[32]	China	277/238	57 ± 11.3/55 ± 10.8	Hospital-based	CAL	CAG	CHD	2.70 (1.52-4.80)1	7
Latronico et al[33]	Italy	15/19	57.7/55.1	Population-based	ABL	CAG	CHD	5.85 (1.03-33.12)	6
Nonnenmacher et al[34]	Germany	45/45	63.5 ± 7.4/63.6 ± 7.4	Hospital-based	CAL	CAG	CHD	3.2 (1.2-9.0)1	7
Rech et al[35]	Brazil	58/57	59.3/70	Hospital-based	PPD	ECG	MI	1.8 (0.7-4.7)1	6
Ge et al[36]	China	13/30	55.1 ± 4.8/51.2 ± 4.7	Hospital-based	CAL	CAG	CHD	2.53 (1.01-6.32)1	6
Meng et al[37]	China	150/150	71.2 ± 4.6/71.9 ± 4.7	Population-based	ABL	C	CHD	2.95 (1.74-5.02)	5
Wu et al[38]	China	77/75	53.81 ± 8.25/ 51.14 ± 6.44	Hospital-based	CAL	CAG	CHD	2.18 (1.52-3.13)	5
Zamirian et al[39]	Iran	80/80	54.0 ± 8.7/51.9 ± 9.4	Hospital-based	CAL	ECG	MI	3.18 (1.37-7.42)1	6
Zhu et al[40]	China	98/104	61.34 ± 9.63	Population-based	CAL	C	MI	11.43 (2.59-50.34)	5
Dong et al[41]	China	161/162	33-66/30-70	Population-based	ABL	CAG	CHD	5.74 (2.07-15.90)1	7
Ma et al[42]	China	146/257	45-72	Hospital-based	CAL	CAG	CHD	2.36 (1.49-3.73)	5
Oikarinen et al[43]	Kuwait	88/88	48.8 ± 10.0/47.0 ± 11.6	Hospital-based	ABL	C	CHD	19.69 (19.36-20.02)	6
Sun et al[44]	China	167/242	68.28 ± 10.53/ 50.18 ± 10.56	Hospital-based	CAL	CAG	CHD	9.10 (0.87-95.07)1	7
Willershausen et al[45]	Germany	125/125	61.8 ± 10.4/63.4 ± 10.7	Population-based	CAL	ECG	MI	3.65 (2.02-6.56)1	7
Bokhari et al[46]	Pakistan	45/35	41.67 ± 5.11/ 40.31 ± 6.97	Hospital-based	PPD	CAG	CHD	6.37 (1.26-32.27)	6
Chen[47]	China	46/34	38-68/35-66	Hospital-based	ABL	CAG	CHD	9.87 (3.50-27.82)	4
Sikka et al[48]	India	100/100	54.97 ± 7.97/ 55.1 ± 8.08	Population-based	CPI	CAG	CHD	2.66 (1.50-4.71)	7
Ashraf et al[49]	Pakistan	145/145	53.3 ± 12.3/51.7 ± 11.6	Hospital-based	CPI	C	CHD	1.20 (0.93-1.55)1	7
Zhang et al[50]	China	162/162	66.7/66.0	Hospital-based	Q	CAG	CHD	2.16 (1.65-2.83)1	6

¹Adjusted OR and 95%CI. PD: Periodontal disease; CHD: Coronary heart disease; NOS: Newcastle-Ottawa Scale; CAG: Coronary arteriography; ECG: Electrocardiograph; MI: Myocardial infarction; CAL: Clinical attachment loss; PPD: Periodontal pocket depth; ABL: Alveolar bone loss; CPI: Community periodontal index; PI: Periodontal index; Q: Questionnaire; C: Cardiologist.

Table 2 Adjustments in case-control studies included in this meta-analysis

Ref.	Adjustment
López et al[14]	DM, systolic blood pressure, and smoking
Rutger Persson et al[17]	Smoking
Geerts et al[18]	Age, gender, smoking, DM, hypertension, hyperlipidemia, diet, and alcohol
Montebugnoli et al[19]	Age, smoking, DM, hypertension, high/low density lipoprotein, CRP, leukocytes, BMI, social class
Renvert et al[20]	Smoking
Buhlin et al[22]	Age, gender, smoking, DM, BMI, education, place of birth
Wang et al[24]	Gender, age, BMI, smoking, hypertension, DM, blood lipid, CRP, white blood count, and fibrinogen
Andriankaja et al[25]	Age, gender, hypertension, cholesterol, DM, and smoking
Briggs et al[27]	Smoking, education, alcohol, BMI, exercise, unemployment, hobby, plaque, and CRP
Geismar et al[28]	Gender, smoking, DM, and education
Spahr et al[30]	Age, sex, BMI, smoking, alcohol, DM, hypertension, hyperlipoproteinemia, education, exercise, and statin intake
Zhang et al[32]	Smoking, age, gender, BMI, hypertension, DM, high-density lipoproteincholesterol, total Cholesterol, total glycerin
Nonnenmacher et al[34]	Smoking and BMI
Rech et al[35]	Age, gender, smoking, DM
Ge et al[36]	Blood pressure and BMI
Zamirian et al[39]	Smoking and alcohol
Dong et al[41]	Smoking, age, and education
Sun et al[44]	Age and BMI
Willershausen et al[45]	Age, gender, and smoking
Ashraf et al[49]	Age, gender, and education
Zhang et al[50]	Age, gender, smoking, alcohol, hypertension, and BMI

DM: Diabetes mellitus; BMI: Body mass index; CRP: C-reactive protein.

Table 3 Results of overall and subgroups analyses of pooled odds ratios and 95%CIs

Total and subgroup	No. of trials	Heterogeneity		Model	Meta-analysis
		I2 (%)	P		OR	95%CI	P
Total	38	98.59	< 0.001	Random	3.79	2.23-6.43	< 0.001
Adjustment for covariates
Yes	21	66.02	< 0.001	Random	2.72	2.13-3.46	< 0.001
No	17	98.68	< 0.001	Random	4.62	2.10-10.18	< 0.001
Source of control
HB	22	98.5	< 0.001	Random	4.04	2.00-8.12	< 0.001
PB	16	80.38	< 0.001	Random	3.08	2.23-4.26	< 0.001
Methodological quality (NOS)
< 6	11	83.28	< 0.001	Random	3.38	1.75-6.52	< 0.001
≥ 6	27	98.73	< 0.001	Random	4.16	2.71-6.40	< 0.001
End point
CHD	31	98.75	< 0.001	Random	3.63	2.00-6.59	< 0.001
MI	7	70.15	< 0.001	Random	4.12	2.35-7.22	< 0.001
Assessment of PD
ABL	8	97.93	< 0.001	Random	5.57	1.90-16.33	< 0.001
CAL	10	0	0.5	Fixed	2.54	2.13-3.04	< 0.001
CPI	5	90.24	< 0.001	Random	2.76	1.45-5.23	< 0.001
PI	5	91.95	< 0.001	Random	3.12	1.38-7.05	< 0.001
PPD	8	0	0.76	Fixed	3.55	2.39-5.27	< 0.001
Questionnaire	2	0	0.86	Fixed	2.19	1.73-2.77	< 0.001
Assessment of CHD
CAG	22	73.04	< 0.001	Random	2.85	2.23-3.64	< 0.001
Cardiologists	10	99	< 0.001	Random	5.09	1.71-15.14	< 0.001
ECG	6	60.72	0.03	Random	3.55	2.06-6.12	< 0.001
Ethnicity
America	4	88.24	< 0.001	Random	4.75	1.50-15.02	0.01
Asia	23	99.01	< 0.001	Random	3.46	1.73-6.94	< 0.001
Europe	11	56.82	0.01	Random	3.81	2.46-5.91	< 0.001

PD: Periodontal disease; CHD: Coronary heart disease; NOS: Newcastle-Ottawa Scale; OR: Odds ratio; CAG: Coronary arteriography; ECG: Electrocardiograph; MI: Myocardial infarction; CAL: Clinical attachment loss; PPD: Periodontal pocket depth; ABL: Alveolar bone loss; CPI: Community periodontal index; PI: Periodontal index.