Association between chronic periodontitis and herpes viruses: A review of the literature.
Abstract
Objective: This research aims to analyze the available spe-cialized literature concerning the association between Herpesviruses [Cytomegalovirus (CMV), Epstein Barr virus (EBV), Herpes Simplex virus (HSV)] and chronic periodontitis to clarify the possible role of these microorganisms in the progression and severity of the disease. Materials and Methods: A search for scientific articles was carried out in March 2019 in the main metasearch engines: PubMed /MEDLINE, SciELO, EBSCO, and the Trip search engine, to select articles according to the exclusion and inclusion criteria. The analysis of the articles was carried out through a data matrix expressed in frequency tables using descriptive statistics with measures of central tendency, dispersion, and correlation. Results: The results of this study show that the presence of CMV, EBV, and HSV in patients with chronic periodontitis is related to an increase in clinical parameters such as probing pocket depth (PD), clinical insertion loss (CIL) and bleeding on probing (BOP), in 96%, 60% and 40% of the studies, respectively, for HCMV; 96.55% (PD), 51.72% (CIL), and 48.28% (BOP) for EBV, and 80% (PD), 90% (CIL), and 60% (BOP) for HSV. The average prevalence of EBV, HCMV, and HSV was 46.3%, 35.4%, and 40.1%, respectively. Conclusions: EBV, CMV, and HSV could be associated with the progression and severity of periodontal disease as they are related to a greater probing depth, greater clinical insertion loss, and greater bleeding on probing. EBV presented a higher prevalence in the reviewed literature. More clinical studies are needed to verify a direct relationship between EBV, HSV, CMV, and periodontal disease, to confirm the trends observed in this work.
References
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28. Ling LJ, Ho CC, Wu CY, Chen YT, Hung SL. Association between human herpesviruses and the severity of periodontitis. J Periodontol. 2004;75(11):1479-85.
29. Tantivanich S, Laohapand P, Thaweeboon S, Desakorn V, Wuthinuntiwong P, Chalermtaranukul S, Pansri P, Amarapal P, Balachandra K, Chantratita W, Dhepakson P. Prevalence of cytomegalovirus, human herpesvirus-6, and Epstein-Barr virus in periodontitis patients and healthy subjects in the Thai population. Southeast Asian J Trop Med Public Health. 2004;35(3):635-40.
30. Idesawa M, Sugano N, Ikeda K, Oshikawa M, Takane M, Seki K, Ito K. Detection of Epstein-Barr virus in saliva by real-time PCR. Oral Microbiol Immunol. 2004;19(4):230-2.
31. Klemenc P, Skalerič U, Artnik B, Nograšek P, Marin J. Prevalence of some herpesviruses in gingival crevicular fluid. Journal of clinical virology. 2005; 34(2), 147-152.
32. Konstantinidis A, Sakellari D, Papa A. and Antoniadis, A. Real‐time polymerase chain reaction quantification of Epstein–Barr virus in chronic periodontitis patients. J Periodon Res. 2005; 40: 294-8.
33. Wu YM, Yan J, Chen LL, Sun WL, Gu ZY. Infection frequency of Epstein-Barr virus in subgingival samples from patients with different periodontal status and its correlation with clinical parameters. J Zhejiang Univ Sci B. 2006;7(11):876-83.
34. Moghim SH, Chalabi M, Abed AM, Rezaei F, Tamizifar H. Prevalence of Epstein-Barr virus type 1 in patients with chronic periodontitis by nested-PCR. Pak J Biol Sci. 2007;10(24):4547-50.
35. Saygun I, Kubar A, Şahin S, Şener K, Slots J. Quantitative analysis of association between herpesviruses and bacterial pathogens in periodontitis. J Periodontal Res. 2008; 43(3):352–359
36. Botero JE, Vidal C, Contreras A, Parra B. Comparison of nested polymerase chain reaction (PCR), real‐time PCR and viral culture for the detection of cytomegalovirus in subgingival samples. Oral Microbiol Immunol.2008;3(3), 239-44.
37. Rotola A, Cassai E, Farina R, Caselli E, Gentili V, Lazzarotto T, Trombelli L. Human herpesvirus 7, Epstein-Barr virus and human cytomegalovirus in periodontal tissues of periodontally diseased and healthy subjects. J Clin Periodontol. 2008;35(10):831-7.
38. Combs DR, Reilly EA, Dawson III DR, Avdiushko SA, Danaher RJ, & Miller CS. Detection of human cytomegalovirus in dental plaque from individual periodontal sites by real-time polymerase chain reaction. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. 2008; 106(6), 840-44.
39. Chalabi M, Moghim S, Mogharehabed A, Najafi F, Rezaie F. EBV and CMV in chronic periodontitis: a prevalence study. Arch Virol. 2008;153(10):1917-9.
40. Nishiyama SA, Nakano V, Velásquez-Melendez G, Avila-Campos MJ. Occurrence of herpes simplex virus 1 and three periodontal bacteria in patients with chronic periodontitis and necrotic pulp. Can J Microbiol. 2008;54(4):326-30.
41. Grenier G, Gagnon G, Grenier D. Detection of herpetic viruses in gingival crevicular fluid of patients suffering from periodontal diseases: prevalence and effect of treatment. Oral Microbiol Immunol. 2009;24(6):506-9.
42. Chalabi M, Rezaie F, Moghim S, Mogharehabed A, Rezaei M, Mehraban B. Periodontopathic bacteria and herpesviruses in chronic periodontitis. Mol Oral Microbiol. 2010;25(3):236-40.
43. Dawson DR 3rd, Wang C, Danaher RJ, Lin Y, Kryscio RJ, Jacob RJ, Miller CS. Salivary levels of Epstein-Barr virus DNA correlate with subgingival levels, not severity of periodontitis. Oral Dis. 2009;15(8):554-9.
44. Bilichodmath S, Mangalekar SB, Sharma DC, Prabhakar AK, Reddy SB, Kalburgi NB, Patil SR, Bhat K. Herpesviruses in chronic and aggressive periodontitis patients in an Indian population. J Oral Sci. 2009;51(1):79-86.
45. Saygun I, Kubar A, Ozdemir A, Slots J. Periodontitis lesions are a source of salivary cytomegalovirus and Epstein-Barr virus. J Periodontal Res. 2005;40(2):187-91.
46. Monzón J, Acuña M, Canga E, Ortega S. Prevalencia de herpes virus en bolsas periodontales de pacientes asistidos en la Cátedra de Periodoncia de la FOUNNE / Prevalence of herpes virus in periodontal pockets of patients assisted at the Periodontics Department, FOUNNE. Rev. Fundac Juan Jose Carraro.2011;16(34):36-49.
47. Sharma R, Padmalatha O, Kaarthikeyan G, Jayakumar ND, Varghese S, Sherif K. Comparative analysis of presence of Cytomegalovirus (CMV) and Epsteinbarr virus -1 (EBV-1) in cases of chronic periodontitis and aggressive periodontitis with controls. Indian J Dent Res. 2012;23(4):454-8.
48. Thomasini RL, Bonon SH, Durante P, Costa SC. Correlation of cytomegalovirus and human herpesvirus 7 with CD3+ and CD3+ CD4+ cells in chronic periodontitis patients. J Periodontal Res. 2012;47(1):114-120.
49. Vincent-Bugnas S, Vitale S, Mouline CC, Khaali W, Charbit Y, Mahler P, Prêcheur I, Hofman P, Maryanski JL, Doglio A. EBV infection is common in gingival epithelial cells of the periodontium and worsens during chronic periodontitis. PLoS One. 2013;8(12):e80336.
50. Petrović SM, Zelić K, Milasin J, Popović B, Pucar A, Zelić O. Detection of herpes simplex virus type 1 in gingival crevicular fluid of gingival sulcus/periodontal pocket using polymerase chain reaction. Srp Arh Celok Lek. 2014;142(5-6):296-300.
51. Kato A, Imai K, Ochiai K, Ogata Y. Prevalence and quantitative analysis of Epstein-Barr virus DNA and Porphyromonas gingivalis associated with Japanese chronic periodontitis patients. Clin Oral Investig. 2015;19(7):1605-10.
52. Khosropanah H, Karandish M, Ziaeyan M, Jamalidoust M. Quantification of Epstein-Barr Virus and Human Cytomegalovirus in Chronic Periodontal Patients. Jundishapur J Microbiol. 2015;8(6):e18691.
53. Kazi MMAG, Bharadwaj R. Role of herpesviruses in chronic periodontitis and their association with clinical parameters and in increasing severity of the disease. Eur J Dent. 2017;11(3):299-304.
2. Hernández HH. Herpes Simplex Virus 1, Cytomegalovirus and Epstein Barr Virus Detection in Patients with Chronic and Aggressive Periodontitis. Open Access Library Journal. 2016;3(03):1.
3. Papone V, Verolo C, Zaffaroni L, Batlle A, Capó C, Bueno L, Gamonal J, Silva, N, Soria S. Detección y prevalencia de patógenos periodontales de una población con periodontitis crónica en Uruguay mediante metodología convencional y metagenómica. ODONTOESTOMATOLOGÍA. 2015; XVII(25): 23-32.
4. Ishikawa I. Host responses in periodontal diseases: a preview. Periodontol 2000. 2007; 43:9-13.
5. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
6. Hernández R, Fernández C, Baptista P. Metodología de la investigación. México: McGraw-Hill, 2010.
7. Wu YM, Yan J, Ojcius DM, Chen LL, Gu ZY, Pan JP. Correlation between infections with different genotypes of human cytomegalovirus and Epstein-Barr virus in subgingival samples and periodontal status of patients. J Clin Microbiol. 2007;45(11):3665-70.
8. Zhu C, Li F, Wong MC, Feng XP, Lu HX, Xu W. Association between Herpesviruses and Chronic Periodontitis: A Meta-Analysis Based on Case-Control Studies. PLoS One. 2015;10(12):e0144319.
9. Contreras A, Botero JE, Slots J. Biology and pathogenesis of cytomegalovirus in periodontal disease. Periodontol. 2000;64(1):40-56.
10. Binshabaib M, ALHarthi SS, Salehpoor D, Michelogiannakis D, Javed F. Contribution of herpesviruses in the progression of periodontal and peri‐implant diseases in systemically healthy individuals. Rev Med Virol. 2018; 28:e1996.
11. Shah R, Mehta DS. Prevalence of herpesviruses in gingivitis and chronic periodontitis: relationship to clinical parameters and effect of treatment. J Indian Soc Periodontol. 2016;20(3):279-85.
12. Kazi MM, Bharadwaj R, Bhat K, Happy D. Association of Herpes Viruses with Mild, Moderate and Severe Chronic Periodontitis. J Clin Diagn Res. 2015;9(7):DC05-8.
13. Mombelli A. Microbial colonization of the periodontal pocket and its significance for periodontal therapy. Periodontology 2000. 2018; 76(1), 85-96.
14. Srivastava AK, Shukla S, Srivastava P, Dhole TN, Nayak MT, Nayak A, Mathur A. Real time detection and quantification of Epstein Barr virus in different grades of oral gingivitis and periodontitis patients. J Exp Ther Oncol. 2019;13(1):9-14.
15. Slots J. Periodontal herpesviruses: prevalence, patho-genicity, systemic risk. Periodontology 2000. 2015;69(1), 28-45.
16. Contreras A, Botero JE, Slots J. Biology and pathogenesis of cytomegalovirus in periodontal disease. Periodontol 2000. 2014;64(1):40-56.
17. Kato A, Imai K, Ochiai K, Ogata Y. Higher prevalence of Epstein-Barr virus DNA in deeper periodontal pockets of chronic periodontitis in Japanese patients. PLoS One. 2013;8(8):e71990.
18. Das S, Krithiga GS, Gopalakrishnan S. Detection of human herpes viruses in patients with chronic and aggressive periodontitis and relationship between viruses and clinical parameters. J Oral Maxillofac Pathol.2012;16(2):203-9.
19. Contreras A, Botero, JE, Slots J. Biology and pathogenesis of cytomegalovirus in periodontal disease. Periodontology 2000. 2014; 64(1), 40-56.
20. Botero J E, Parra B, Jaramillo A, Contreras A. Subgingival human cytomegalovirus correlates with increased clinical periodontal parameters and bacterial coinfection in periodontitis. Journal of periodontology, 2007; 78(12), 2303-10.
21. Imbronito AV, Okuda OS, Maria de Freitas N, Moreira Lotufo RF, Nunes FD. Detection of herpesviruses and periodontal pathogens in subgingival plaque of patients with chronic periodontitis, generalized aggressive periodontitis, or gingivitis. J Periodontol. 2008;79(12):2313-21.
22. Bilder L, Elimelech R, Szwarcwort-Cohen M, Kra-Oz Z, Machtei EE. The prevalence of human herpes viruses in the saliva of chronic periodontitis patients compared to oral health providers and healthy controls. Arch Virol. 2013; 158:1221–6.
23. Imai K, Ogata Y. How Does Epstein-Barr Virus Contribute to Chronic Periodontitis? Int J Mol Sci. 2020;21(6):1940.
24. Bertoldi C, Pellacani C, Lalla M, Consolo U, Pinti M, Cortellini P, Cossarizza A. Herpes Simplex I virus impairs regenerative outcomes of periodontal regenerative therapy in intrabony defects. A pilot study. Journal of clinical periodontology. 2012; 39(4), 385-92.
25. Ivanovska-Stojanoska M, Popovska M, Anastasovska V, Kocova M, Zendeli-Bedzeti L, Dimova C, Taseva A. Detection of Virus Herpes Simplex Type 1 in Patients with Chronic Periodontal Disease. Open Access Maced J Med Sci. 2018;6(9):1737-41.
26. Saygun I, Sahin S, Ozdemir A, Kurtiş B, Yapar M, Kubar A, Ozcan G. Detection of human viruses in patients with chronic periodontitis and the relationship between viruses and clinical parameters. J Periodontol. 2002;73(12):1437-43.
27. Li Y, Zhang JC, Zhang YH. [The association between infection of Epstein-Barr virus and chronic periodontitis]. Zhonghua Kou Qiang Yi Xue Za Zhi. 2004;39(2):146-8.
28. Ling LJ, Ho CC, Wu CY, Chen YT, Hung SL. Association between human herpesviruses and the severity of periodontitis. J Periodontol. 2004;75(11):1479-85.
29. Tantivanich S, Laohapand P, Thaweeboon S, Desakorn V, Wuthinuntiwong P, Chalermtaranukul S, Pansri P, Amarapal P, Balachandra K, Chantratita W, Dhepakson P. Prevalence of cytomegalovirus, human herpesvirus-6, and Epstein-Barr virus in periodontitis patients and healthy subjects in the Thai population. Southeast Asian J Trop Med Public Health. 2004;35(3):635-40.
30. Idesawa M, Sugano N, Ikeda K, Oshikawa M, Takane M, Seki K, Ito K. Detection of Epstein-Barr virus in saliva by real-time PCR. Oral Microbiol Immunol. 2004;19(4):230-2.
31. Klemenc P, Skalerič U, Artnik B, Nograšek P, Marin J. Prevalence of some herpesviruses in gingival crevicular fluid. Journal of clinical virology. 2005; 34(2), 147-152.
32. Konstantinidis A, Sakellari D, Papa A. and Antoniadis, A. Real‐time polymerase chain reaction quantification of Epstein–Barr virus in chronic periodontitis patients. J Periodon Res. 2005; 40: 294-8.
33. Wu YM, Yan J, Chen LL, Sun WL, Gu ZY. Infection frequency of Epstein-Barr virus in subgingival samples from patients with different periodontal status and its correlation with clinical parameters. J Zhejiang Univ Sci B. 2006;7(11):876-83.
34. Moghim SH, Chalabi M, Abed AM, Rezaei F, Tamizifar H. Prevalence of Epstein-Barr virus type 1 in patients with chronic periodontitis by nested-PCR. Pak J Biol Sci. 2007;10(24):4547-50.
35. Saygun I, Kubar A, Şahin S, Şener K, Slots J. Quantitative analysis of association between herpesviruses and bacterial pathogens in periodontitis. J Periodontal Res. 2008; 43(3):352–359
36. Botero JE, Vidal C, Contreras A, Parra B. Comparison of nested polymerase chain reaction (PCR), real‐time PCR and viral culture for the detection of cytomegalovirus in subgingival samples. Oral Microbiol Immunol.2008;3(3), 239-44.
37. Rotola A, Cassai E, Farina R, Caselli E, Gentili V, Lazzarotto T, Trombelli L. Human herpesvirus 7, Epstein-Barr virus and human cytomegalovirus in periodontal tissues of periodontally diseased and healthy subjects. J Clin Periodontol. 2008;35(10):831-7.
38. Combs DR, Reilly EA, Dawson III DR, Avdiushko SA, Danaher RJ, & Miller CS. Detection of human cytomegalovirus in dental plaque from individual periodontal sites by real-time polymerase chain reaction. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. 2008; 106(6), 840-44.
39. Chalabi M, Moghim S, Mogharehabed A, Najafi F, Rezaie F. EBV and CMV in chronic periodontitis: a prevalence study. Arch Virol. 2008;153(10):1917-9.
40. Nishiyama SA, Nakano V, Velásquez-Melendez G, Avila-Campos MJ. Occurrence of herpes simplex virus 1 and three periodontal bacteria in patients with chronic periodontitis and necrotic pulp. Can J Microbiol. 2008;54(4):326-30.
41. Grenier G, Gagnon G, Grenier D. Detection of herpetic viruses in gingival crevicular fluid of patients suffering from periodontal diseases: prevalence and effect of treatment. Oral Microbiol Immunol. 2009;24(6):506-9.
42. Chalabi M, Rezaie F, Moghim S, Mogharehabed A, Rezaei M, Mehraban B. Periodontopathic bacteria and herpesviruses in chronic periodontitis. Mol Oral Microbiol. 2010;25(3):236-40.
43. Dawson DR 3rd, Wang C, Danaher RJ, Lin Y, Kryscio RJ, Jacob RJ, Miller CS. Salivary levels of Epstein-Barr virus DNA correlate with subgingival levels, not severity of periodontitis. Oral Dis. 2009;15(8):554-9.
44. Bilichodmath S, Mangalekar SB, Sharma DC, Prabhakar AK, Reddy SB, Kalburgi NB, Patil SR, Bhat K. Herpesviruses in chronic and aggressive periodontitis patients in an Indian population. J Oral Sci. 2009;51(1):79-86.
45. Saygun I, Kubar A, Ozdemir A, Slots J. Periodontitis lesions are a source of salivary cytomegalovirus and Epstein-Barr virus. J Periodontal Res. 2005;40(2):187-91.
46. Monzón J, Acuña M, Canga E, Ortega S. Prevalencia de herpes virus en bolsas periodontales de pacientes asistidos en la Cátedra de Periodoncia de la FOUNNE / Prevalence of herpes virus in periodontal pockets of patients assisted at the Periodontics Department, FOUNNE. Rev. Fundac Juan Jose Carraro.2011;16(34):36-49.
47. Sharma R, Padmalatha O, Kaarthikeyan G, Jayakumar ND, Varghese S, Sherif K. Comparative analysis of presence of Cytomegalovirus (CMV) and Epsteinbarr virus -1 (EBV-1) in cases of chronic periodontitis and aggressive periodontitis with controls. Indian J Dent Res. 2012;23(4):454-8.
48. Thomasini RL, Bonon SH, Durante P, Costa SC. Correlation of cytomegalovirus and human herpesvirus 7 with CD3+ and CD3+ CD4+ cells in chronic periodontitis patients. J Periodontal Res. 2012;47(1):114-120.
49. Vincent-Bugnas S, Vitale S, Mouline CC, Khaali W, Charbit Y, Mahler P, Prêcheur I, Hofman P, Maryanski JL, Doglio A. EBV infection is common in gingival epithelial cells of the periodontium and worsens during chronic periodontitis. PLoS One. 2013;8(12):e80336.
50. Petrović SM, Zelić K, Milasin J, Popović B, Pucar A, Zelić O. Detection of herpes simplex virus type 1 in gingival crevicular fluid of gingival sulcus/periodontal pocket using polymerase chain reaction. Srp Arh Celok Lek. 2014;142(5-6):296-300.
51. Kato A, Imai K, Ochiai K, Ogata Y. Prevalence and quantitative analysis of Epstein-Barr virus DNA and Porphyromonas gingivalis associated with Japanese chronic periodontitis patients. Clin Oral Investig. 2015;19(7):1605-10.
52. Khosropanah H, Karandish M, Ziaeyan M, Jamalidoust M. Quantification of Epstein-Barr Virus and Human Cytomegalovirus in Chronic Periodontal Patients. Jundishapur J Microbiol. 2015;8(6):e18691.
53. Kazi MMAG, Bharadwaj R. Role of herpesviruses in chronic periodontitis and their association with clinical parameters and in increasing severity of the disease. Eur J Dent. 2017;11(3):299-304.
Published
2020-06-30
How to Cite
OÑATE, Héctor et al.
Association between chronic periodontitis and herpes viruses: A review of the literature..
Journal of Oral Research, [S.l.], v. 9, n. 3, p. 234-244, june 2020.
ISSN 0719-2479.
Available at: <https://joralres.com/index.php/JOralRes/article/view/joralres.2020.040>. Date accessed: 25 apr. 2024.
doi: https://doi.org/10.17126/joralres.2020.040.
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