Association of oral Epstein‑Barr virus with periodontal health in Japanese adults

Su,Cheng-Yih; Shigeishi,Hideo; Murodumi,Hiroshi; Sugiyama,Masaru; Ohta,Kouji; Takemoto,Toshinobu

doi:10.3892/etm.2021.10199

Association of oral Epstein‑Barr virus with periodontal health in Japanese adults

Authors:
- Cheng-Yih Su
- Hideo Shigeishi
- Hiroshi Murodumi
- Masaru Sugiyama
- Kouji Ohta
- Toshinobu Takemoto
View Affiliations

Affiliations: Department of Oral Health Management, Program of Oral Health Sciences, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima 734‑8553, Japan, Department of Public Oral Health, Program of Oral Health Sciences, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima 734‑8553, Japan, Department of Oral and Maxillofacial Surgery, Program of Dentistry, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima 734‑8553, Japan
Published online on: May 17, 2021 https://doi.org/10.3892/etm.2021.10199
Article Number: 767

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Previous studies have demonstrated that oral Epstein‑Barr virus (EBV) is associated with periodontitis. However, the relationship between periodontitis and oral EBV has not been fully elucidated by reducing the effects of confounding factors. The aim of the present study was to clarify the association between oral Epstein‑Barr virus (EBV) and oral health status among middle‑aged and older Japanese individuals. A total of 124 patients (46 males and 78 females; mean age, 69.2 years; age range, 35‑90 years) who visited Hiroshima University Hospital between October 2018 and December 2019 were recruited into the present study. EBV DNA positivity was determined in 124 oral rinse samples using quantitative PCR. Periodontal disease‑related bacteria were also detected by PCR analysis. EBV DNA was determined as positive in 16 of the 124 enrolled patients (12.9%). No significant difference was identified between EBV DNA and clinical factors (sex, age, remaining teeth, denture use, smoking or medical history). Of the 38 patients with periodontal pockets ≥6 mm, 10 were EBV DNA positive (26.3%). There was a significant association between EBV DNA positivity and probing depth (P=0.01). Additionally, a significant association was identified between bleeding on probing (BOP) and EBV DNA positivity (P=0.03). To investigate the relationship between EBV and periodontal health status, propensity score‑matching was determined between participants without ≥4 mm periodontal pockets and BOP (participants with good periodontal health) and those with ≥4 mm periodontal pockets, BOP or both (participants with poor periodontal health). A total of 35 matched pairs were identified among the patients. Patients with poor periodontal health exhibited a higher EBV DNA positivity rate (25.7%) than those with good periodontal health (0.0%). Additionally, there was a significant association between EBV DNA positivity and periodontal health status (P=0.001). T. denticola‑positive participants exhibited a higher EBV DNA positivity rate than negative participants (17.6 vs. 9.6%). However, there was no significant difference. The results indicated that oral EBV may be markedly associated with periodontitis in middle‑aged and older Japanese individuals.

View Figures

View References

1	Baer R, Bankier AT, Biggin MD, Deininger PL, Farrell PJ, Gibson TJ, Hatfull G, Hudson GS, Satchwell SC, Séguin C, et al: DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature. 310:207–211. 1984.PubMed/NCBI View Article : Google Scholar
2	Houldcroft CJ and Kellam P: Host genetics of Epstein-Barr virus infection, latency and disease. Rev Med Virol. 25:71–84. 2015.PubMed/NCBI View Article : Google Scholar
3	Cohen JI: Epstein-Barr virus infection. N Engl J Med. 343:481–492. 2000.PubMed/NCBI View Article : Google Scholar
4	Epstein MA: Reflections on Epstein-Barr virus: Some recently resolved old uncertainties. J Infect. 43:111–115. 2001.PubMed/NCBI View Article : Google Scholar
5	Hjalgrim H, Askling J, Rostgaard K, Hamilton-Dutoit S, Frisch M, Zhang JS, Madsen M, Rosdahl N, Konradsen HB, Storm HH and Melbye M: Characteristics of Hodgkin's lymphoma after infectious mononucleosis. N Engl J Med. 349:1324–1332. 2003.PubMed/NCBI View Article : Google Scholar
6	Cho WC: Nasopharyngeal carcinoma: Molecular biomarker discovery and progress. Mol Cancer. 6(1)2007.PubMed/NCBI View Article : Google Scholar
7	Shibata D, Tokunaga M, Uemura Y, Sato E, Tanaka S and Weiss LM: Association of Epstein-Barr virus with undifferentiated gastric carcinomas with intense lymphoid infiltration. Lymphoepithelioma-like carcinoma. Am J Pathol. 139:469–474. 1991.PubMed/NCBI
8	Jiang R, Scott RS and Hutt-Fletcher LM: Epstein-Barr virus shed in saliva is high in B-cell-tropic glycoprotein gp42. J Virol. 80:7281–7283. 2006.PubMed/NCBI View Article : Google Scholar
9	Hadinoto V, Shapiro M, Sun CC and Thorley-Lawson DA: The dynamics of EBV shedding implicate a central role for epithelial cells in amplifying viral output. PLoS Pathog. 5(e1000496)2009.PubMed/NCBI View Article : Google Scholar
10	Kamma JJ, Contreras A and Slots J: Herpes viruses and periodontopathic bacteria in early-onset periodontitis. J Clin Periodontol. 28:879–885. 2001.PubMed/NCBI View Article : Google Scholar
11	Imbronito AV, Okuda OS, Maria de Freitas N, Moreira Lotufo RF and Nunes FD: Detection of herpesviruses and periodontal pathogens in subgingival plaque of patients with chronic periodontitis, generalized aggressive periodontitis, or gingivitis. J Periodontol. 79:2313–2321. 2008.PubMed/NCBI View Article : Google Scholar
12	Dawson DR, Wang C, Danaher RJ, Lin Y, Kryscio RJ, Jacob RJ and Miller CS: Real-time polymerase chain reaction to determine the prevalence and copy number of Epstein-Barr virus and cytomegalovirus DNA in subgingival plaque at individual healthy and periodontal disease sites. J Periodontol. 80:1133–1140. 2009.PubMed/NCBI View Article : Google Scholar
13	Zhu C, Li F, Wong MC, Feng XP, Lu HX and Xu W: Association between Herpesviruses and chronic periodontitis: A meta-analysis based on case-control studies. PLoS One. 10(e0144319)2015.PubMed/NCBI View Article : Google Scholar
14	He YQ, Liao XY, Xue WQ, Xu YF, Xu FH, Li FF, Li XZ, Zhang JB, Wang TM, Wang F, et al: Association between environmental factors and oral Epstein-Barr virus DNA loads: A multicenter cross-sectional study in China. J Infect Dis. 219:400–409. 2019.PubMed/NCBI View Article : Google Scholar
15	Dworzański J, Drop B, Kliszczewska E, Strycharz-Dudziak M and Polz-Dacewicz M: Prevalence of Epstein-Barr virus, human papillomavirus, cytomegalovirus and herpes simplex virus type 1 in patients with diabetes mellitus type 2 in south-eastern Poland. PLoS One. 14(e0222607)2019.PubMed/NCBI View Article : Google Scholar
16	Hamada R, Suehiro J, Nakano M, Kikutani T and Konishi K: Development of rapid oral bacteria detection apparatus based on dielectrophoretic impedance measurement method. IET Nanobiotechnol. 5:25–31. 2011.PubMed/NCBI View Article : Google Scholar
17	O'Leary TJ, Drake RB and Naylor JE: The plaque control record. J Periodontol. 43(38)1972.PubMed/NCBI View Article : Google Scholar
18	Shigeishi H, Sugiyama M, Ohta K, Rahman MZ and Takechi M: Higher prevalence and gene amplification of HPV16 in oropharynx as compared to oral cavity. J Appl Oral Sci. 24:397–403. 2016.PubMed/NCBI View Article : Google Scholar
19	Kato A, Imai K, Sato H and Ogata Y: Prevalence of Epstein-Barr virus DNA and Porphyromonas gingivalis in Japanese peri-implantitis patients. BMC Oral Health. 17(148)2017.PubMed/NCBI View Article : Google Scholar
20	Su CY, Shigeishi H, Nishimura R, Ohta K and Sugiyama M: Detection of oral bacteria on the tongue dorsum using PCR amplification of 16S ribosomal RNA and its association with systemic disease in middle-aged and elderly patients. Biomed Rep. 10:70–76. 2019.PubMed/NCBI View Article : Google Scholar
21	Socransky SS, Haffajee AD, Cugini MA, Smith C and Kent RL Jr: Microbial complexes in subgingival plaque. J Clin Periodontol. 25:134–144. 1998.PubMed/NCBI View Article : Google Scholar
22	Slots J and Contreras A: Herpesviruses: A unifying causative factor in periodontitis? Oral Microbiol Immunol. 15:277–280. 2000.PubMed/NCBI View Article : Google Scholar
23	Michalowicz BS, Ronderos M, Camara-Silva R, Contreras A and Slots J: Human herpesviruses and Porphyromonas gingivalis are associated with juvenile periodontitis. J Periodontol. 71:981–988. 2000.PubMed/NCBI View Article : Google Scholar
24	Gao Z, Lv J and Wang M: Epstein-Barr virus is associated with periodontal diseases: A meta-analysis based on 21 case-control studies. Medicine (Baltimore). 96(e5980)2017.PubMed/NCBI View Article : Google Scholar
25	de Souza PH, de Toledo BE, Rapp GE, Zuza EP, Neto CB and Mendes AJ: Reliability of bleeding and non-bleeding on probing to gingival histological features. J Int Acad Periodontol. 5:71–76. 2003.PubMed/NCBI
26	Teughels W, Sliepen I, Quirynen M, Haake SK, Van Eldere J, Fives-Taylor P and Van Ranst M: Human cytomegalovirus enhances A. actinomycetemcomitans adherence to cells. J Dent Res. 86:175–180. 2007.PubMed/NCBI View Article : Google Scholar
27	Srivastava AK, Shukla S, Srivastava P, Dhole TN, Nayak MT, Nayak A and Mathur A: Real time detection and quantification of Epstein Barr virus in different grades of oral gingivitis and periodontitis patients. J Exp Ther Oncol. 13:9–14. 2019.PubMed/NCBI
28	Acharya S, Ekalaksananan T, Vatanasapt P, Loyha K, Phusingha P, Promthet S, Kongyingyoes B and Pientong C: Association of Epstein-Barr virus infection with oral squamous cell carcinoma in a case-control study. J Oral Pathol Med. 44:252–257. 2015.PubMed/NCBI View Article : Google Scholar
29	Singh PN, Natto Z, Yel D, Job J and Knutsen S: Betel quid use in relation to infectious disease outcomes in Cambodia. Int J Infect Dis. 16:e262–e267. 2012.PubMed/NCBI View Article : Google Scholar
30	Saha A and Robertson ES: Epstein-Barr virus-associated B-cell lymphomas: Pathogenesis and clinical outcomes. Clin Cancer Res. 7:3056–3063. 2011.PubMed/NCBI View Article : Google Scholar
31	Tsao SW, Tsang CM, To KF and Lo KW: The role of Epstein-Barr virus in epithelial malignancies. J Pathol. 235:323–333. 2015.PubMed/NCBI View Article : Google Scholar
32	Mao EJ and Smith CJ: Detection of Epstein-Barr virus (EBV) DNA by the polymerase chain reaction (PCR) in oral smears from healthy individuals and patients with squamous cell carcinoma. J Oral Pathol Med. 22:12–17. 1993.PubMed/NCBI View Article : Google Scholar
33	Sand LP, Jalouli J, Larsson PA and Hirsch JM: Prevalence of Epstein-Barr virus in oral squamous cell carcinoma, oral lichen planus, and normal oral mucosa. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 93:586–592. 2002.PubMed/NCBI View Article : Google Scholar