Oral human cytomegalovirus prevalence and its relationships with periodontitis and <i>Porphyromonas gingivalis</i> in Japanese adults: a cross-sectional study

NAKAMURA, Mariko; SHIGEISHI, Hideo; Cheng-Yih, SU; SUGIYAMA, Masaru; OHTA, Kouji

doi:10.1590/1678-7757-2020-00501

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Brasil

Journal of Applied Oral Science

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Brasil

Español English

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Sumário

Original Article • J. Appl. Oral Sci. 28 • 2020 • https://doi.org/10.1590/1678-7757-2020-00501 copy

Oral human cytomegalovirus prevalence and its relationships with periodontitis and Porphyromonas gingivalis in Japanese adults: a cross-sectional study

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective

This study aimed to clarify the association between oral human cytomegalovirus (HCMV) and periodontitis in Japanese adults.

Methodology

In total, 190 patients (75 men and 115 women; mean age, 70.2 years) who visited Hiroshima University Hospital between March 2018 and May 2020 were included. Oral rinse samples were taken to examine the presence of HCMV DNA using real-time polymerase chain reaction (PCR). P. gingivalis was detected by semi-quantitative PCR analysis.

Results

HCMV DNA was present in nine of 190 patients (4.7%). There were significant associations between HCMV presence and the presence of ≥4-mm-deep periodontal pockets with bleeding on probing (BOP) (P<0.01) and ≥6-mm-deep periodontal pockets with BOP (P=0.01). However, no significant relationship was observed between HCMV presence and periodontal epithelial surface area scores. Logistic regression analysis revealed that the presence of ≥4-mm-deep periodontal pockets with BOP was significantly associated with HCMV (odds ratio, 14.4; P=0.01). Propensity score matching was performed between patients presenting ≥4-mm-deep periodontal pockets with BOP (i.e., active periodontitis) and patients without ≥4-mm-deep periodontal pockets with BOP; 62 matched pairs were generated. Patients who had ≥4-mm-deep periodontal pockets with BOP showed a higher rate of HCMV presence (9.7%) than those who lacked ≥4-mm-deep periodontal pockets with BOP (0.0%). There was a significant relationship between HCMV presence and ≥4-mm-deep periodontal pockets with BOP (P=0.03). A significant relationship was found between HCMV/P. gingivalis DNA presence and ≥4-mm-deep periodontal pockets with BOP (P=0.03).

Conclusions

Coinfection of oral HCMV and P. gingivalis was significantly associated with active periodontitis. Moreover, interactions between oral HCMV and P. gingivalis may be related to the severity of periodontal disease.

Human Cytomegalovirus; Periodontitis; Porphyromonas gingivalis; Real-time PCR

Clinical factor (n)	HCMV DNA		P-value
	(-) (n=181)	(+) (n=9)
Age	70.2±11.4	69.0±10.9	0.77
Age in years			0.63
30-39 (2)	2 (100%)	0 (0.0%)
40-49 (7)	6 (85.7%)	1 (14.3%)
50-59 (22)	22 (100%)	0 (0.0%)
60-69 (51)	47 (92.2%)	4 (7.8%)
70-79 (67)	65 (97.0%)	2 (3.0%)
80-89 (38)	36 (94.7%)	2 (5.3%)
90-99 (3)	3 (100%)	0 (0.0%)
Sex
Men (75)	68 (90.7%)	7 (9.3%)	0.03
Women (115)	113 (98.3%)	2 (1.7%)
Heart disease
No (179)	171 (95.5%)	8 (4.5%)	0.42
Yes (11)	10 (90.9%)	1 (9.1%)
Stroke Diabetes
No (184)	176 (95.7%)	8 (4.3%)	0.26
Yes (6)	5 (83.3%)	1 (16.7%)
Hypertension
No (142)	136 (95.8%)	6 (4.2%)	0.69
Yes (48)	45 (93.8%)	3 (6.3%)
Diabetes
No (166)	157 (94.6%)	9 (5.4%)	0.61
Yes (24)	24 (100%)	0 (0.0%)
Hyperlipidemia
No (155)	147 (94.8%)	8 (5.2%)	1.0
Yes (35)	34 (97.1%)	1 (2.9%)
Smoking
Non-smoker (161)	154 (95.7%)	7 (4.3%)	0.63
Current/former smoker (29)	27 (93.1%)	2 (6.9%)
Remaining teeth	23.4±6.2	20.7±6.4	0.07
Denture user
Non-user (142)	135 (95.1%)	7 (4.9%)	1.0
User (48)	46 (95.8%)	2 (4.2%)

Factor (n)	HCMV DNA		P-value
	(-)	(+)
Plaque Control Record scores (%)	35.1±18.2	41.5±18.4	0.33
Probing depth
<4 mm (75)	74 (98.7%)	1 (1.3%)	0.09
≥4 mm and <6 mm (50)	48 (96.0%)	2 (4.0%)
≥6 mm (65)	59 (90.8%)	6 (9.2%)
≥4 mm periodontal pocket with BOP
No (123)	122 (99.2%)	1 (0.8%)	<0.01
Yes (67)	59 (88.1%)	8 (11.9%)
≥6 mm periodontal pocket with BOP
No (145)	142 (97.9%)	3 (2.1%)	0.01
Yes (45)	39 (86.7%)	6 (13.3%)
PISA (mm ² )	201.0±215.9	114.8±85.1	0.46
PESA (mm²)	1219.7±1003.1	1071.6±349.5	0.84

Factor (n)	HCMV(-)/P. gingivalis(-) (n=86)	HCMV(+)/ P. gingivalis(-) (n=1)	HCMV(-)/P. gingivalis(+) (n=95)	HCMV(+)/ P. gingivalis(+) (n=8)	P-value
Plaque Control Record scores (%)	32.1±19.7	25.0	37.6±16.7	44.2±18.5	0.10
Probing depth
<4 mm (75)	46 (53.5%)*	1 (0.0%)	28 (29.5%)	0 (0.0%)	0.01
≥4 mm and <6 mm (50)	22 (25.6%)	0 (0.0%)	26 (27.4%)	2 (25.0%)
≥6 mm (65)	18 (20.9%)	0 (0.0%)	41 (43.2%)*	6 (75.0%)*
≥4 mm periodontal pocket with BOP
No (123)	67 (77.9%)*	1 (100%)	55 (57.9%)	0 (0.0%)	<0.01
Yes (67)	19 (22.1%)	0 (0.0%)	40 (42.1%)*	8 (100%)*
≥6 mm periodontal pocket with BOP
No (145)	74 (86.0%)*	1 (100%)	68 (71.6%)	2 (25.0%)	0.01
Yes (45)	12 (14.0%)	0 (0.0%)	27 (28.4%)	6 (75.0%)*
PISA (mm²)	173.8±148.1	180.8	227.3±264.2	101.6±88.0	0.78
PESA (mm²)	1127.1±304.5	1017	1306.0±1374.2	1080.8±382.0	0.98

Factor (n)	HCMV DNA		P-value
	(-)	(+)
P. gingivalis
Negative (87)	86 (98.9%)	1 (1.1%)	0.04
Positive (103)	95 (92.2%)	8 (7.8%)
Type I fimA
Negative (85)	80 (94.1%)	5 (5.9%)	0.14
Positive (18)	15 (83.3%)	3 (16.7%)
Type Ib fimA
Negative (90)	83 (92.2%)	7 (7.8%)	1.0
Positive (13)	12 (92.3%)	1 (7.7%)
Type II fimA
Negative (2)	2 (100%)	0 (0.0%)	1.0
Positive (101)	93 (92.1%)	8 (7.9%)
Type III fimA
Negative (98)	90 (91.8%)	8 (8.2%)	1.0
Positive (5)	5 (100%)	0 (0.0%)
Type IV fimA
Negative (90)	82 (91.1%)	8 (8.9%)	0.59
Positive (13)	13 (100%)	0 (0.0%)
Type V fimA
Negative (100)	92 (92.0%)	8 (8.0%)	1.0
Positive (3)	3 (100%)	0 (0.0%)

Clinical factor (n)	Patients without ≥4 mm periodontal pocket exhibiting BOP (n=62)	Patients with ≥4 mm periodontal pocket exhibiting BOP (n=62)	P-value
Age	68.4±10.5	69.7±11.3	0.34
Age in years
30-39 (2)	1 (50.0%)	1 (50.0%)	0.95
40-49 (5)	2 (40.0%)	3 (60.0%)
50-59 (14)	8 (57.1%)	6 (42.9%)
60-69 (37)	20 (54.1%)	17 (45.9%)
70-79 (45)	22 (48.9%)	23 (51.1%)
80-89 (21)	9 (42.9%)	12 (57.1%)
Sex
Male (57)	29 (50.9%)	28 (49.1%)	1.0
Female (67)	33 (49.3%)	34 (50.7%)
Heart disease
No (117)	58 (49.6%)	59 (50.4%)	1.0
Yes (7)	4 (57.1%)	3 (42.9%)
Stroke
No (120)	60 (50.0%)	60 (50.0%)	1.0
Yes (4)	2 (50.0%)	2 (50.0%)
Hypertension
No (90)	44 (48.9%)	46 (51.1%)	0.84
Yes (34)	18 (52.9%)	16 (47.1%)
Diabetes
No (108)	54 (50.0%)	54 (50.0%)	1.0
Yes (16)	8 (50.0%)	8 (50.0%)
Hyperlipidemia
No (99)	49 (49.5%)	50 (50.5%)	1.0
Yes (25)	13 (52.0%)	12 (48.0%)
Smoking
Non-smoker (99)	49 (49.5%)	50 (50.5%)	1.0
Current/former smoker (25)	13 (52.0%)	12 (48.0%)
Remaining teeth	23.5±5.9	23.3±6.0	0.70
Denture user
Non-user (93)	47 (50.5%)	46 (49.5%)	1.0
User (31)	15 (48.4%)	16 (51.6%)

Clinical factor (n)	Patients without ≥4 mm periodontal pocket exhibiting BOP (n=62)	Patients with ≥4 mm periodontal pocket exhibiting BOP (n=62)	P-value
HCMV
Negative (118)	62 (52.5%)	56 (47.5%)	0.03
Positive (6)	0 (0.0%)	6 (100%)
*P. gingivalis*
Negative (55)	37 (67.3%)	18 (32.7%)	<0.01
Positive (69)	25 (36.2%)	44 (63.8%)
*HCMV(+)/P. gingivalis(+)*
Yes (6)	0 (0.0%)	6 (100%)	0.03
No (118)	62 (52.5%)	56 (47.5%)

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[1] Corresponding address: Dr Hideo Shigeishi Hiroshima University - Graduate School of Biomedical and Health Sciences - Program of Oral Health Sciences - Department of Public Oral Health, 1-2-3 - Kasumi - Minami-ku - Hiroshima 734-8553 - Japan. Phone: +81-82-257-5945 - Fax: +81-82-257-5945 e-mail: shige@hiroshima-u.ac.jp