Skip to main content
Top
Published in: BMC Oral Health 1/2021

01-12-2021 | Epstein-Barr Virus | Research

Detection of Epstein-Barr virus encoded small RNA genes in oral squamous cell carcinoma and non-cancerous oral cavity samples

Authors: Arghavan Zebardast, Yousef Yahyapour, Maryam Seyed Majidi, Mohammad Chehrazi, Farzin Sadeghi

Published in: BMC Oral Health | Issue 1/2021

Login to get access

Abstract

Background

Epstein-Barr Virus (EBV) is a human oncogenic virus that can lead to cancer in lymphoid and epithelial cells and is one of the hypothesized causes of oral cavity lesions including oral squamous cell carcinoma (OSCC), but the etiological association remains undetermined. The present investigation aimed to explore the EBV presence, viral load, and EBV-encoded small RNA (EBER) sequence variation in tissue samples of patients with OSCC and other oral cavity lesions including oral lichen planus (OLP), and oral irritation fibroma (OIF).

Methods

In total, 88 oral cavity samples (23 with OSCC, 29 with OLP, and 36 with OIF diagnosis) were examined by Real-Time PCR technique and some of them were sequenced.

Results

Viral EBER sequence was detected in 6 out of the 23 OSCC (31.4%), 6 out of the 29 OLP (20.7%), and 3 out of the 36 OIF cases (8.3%). The mean EBV copy number was higher in OSCC samples (1.2 × 10−2 ± 1.3 × 10−2 copies/cell) compared to OLP (2.2 × 10−3 ± 2.6 × 10−3 copies/cell) and OIF (2.4 × 10−4 ± 2.0 × 10−4 copies/cell) samples, although this difference was not statistically significant (P = 0.318). The EBER gene was amplified and sequenced in 5 OSCC, 3 OLP, and 2 OIF samples with high EBV viral load. One OSCC, two OLP, and two OIF isolates showed different nucleotide variations compared with EBV-WT and AG876 prototype sequences: C6834T, C6870T, C6981T, C7085T, C7085G, and C7094T.

Conclusion

In our study the presence of more than one genome copies per tumor cell indicates the possible role of EBV infection in oral cancers. However, more studies should be conducted to clarify the role of EBV in OSCC carcinogenesis.
Literature
1.
go back to reference Massano J, Regateiro FS, Januário G, Ferreira A. Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 2006;102(1):67–76.CrossRef Massano J, Regateiro FS, Januário G, Ferreira A. Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 2006;102(1):67–76.CrossRef
2.
go back to reference Dumache R. Early diagnosis of oral squamous cell carcinoma by Salivary microRNAs. Clin Lab. 2017;63(11):1771–6.PubMed Dumache R. Early diagnosis of oral squamous cell carcinoma by Salivary microRNAs. Clin Lab. 2017;63(11):1771–6.PubMed
3.
go back to reference Chiou S-H, Yu C-C, Huang C-Y, Lin S-C, Liu C-J, Tsai T-H, et al. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res. 2008;14(13):4085–95.PubMedCrossRef Chiou S-H, Yu C-C, Huang C-Y, Lin S-C, Liu C-J, Tsai T-H, et al. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res. 2008;14(13):4085–95.PubMedCrossRef
4.
go back to reference Reichart P, Nguyen X. Betel quid chewing, oral cancer and other oral mucosal diseases in Vietnam: a review. J Oral Pathol Med. 2008;37(9):511–4.PubMedCrossRef Reichart P, Nguyen X. Betel quid chewing, oral cancer and other oral mucosal diseases in Vietnam: a review. J Oral Pathol Med. 2008;37(9):511–4.PubMedCrossRef
5.
go back to reference Marur S, Forastiere AA, editors. Head and neck squamous cell carcinoma: update on epidemiology, diagnosis, and treatment. Mayo Clinic Proceedings; 2016: Elsevier. Marur S, Forastiere AA, editors. Head and neck squamous cell carcinoma: update on epidemiology, diagnosis, and treatment. Mayo Clinic Proceedings; 2016: Elsevier.
6.
go back to reference Goldstein BY, Chang S-C, Hashibe M, La Vecchia C, Zhang Z-F. Alcohol consumption and cancer of the oral cavity and pharynx from 1988 to 2009: an update. ECP. 2010;19(6):431. Goldstein BY, Chang S-C, Hashibe M, La Vecchia C, Zhang Z-F. Alcohol consumption and cancer of the oral cavity and pharynx from 1988 to 2009: an update. ECP. 2010;19(6):431.
7.
go back to reference Khan A, Farah CS, Savage NW, Walsh LJ, Harbrow DJ, Sugerman PB. Th1 cytokines in oral lichen planus. J Oral Pathol Med. 2003;32(2):77–83.PubMedCrossRef Khan A, Farah CS, Savage NW, Walsh LJ, Harbrow DJ, Sugerman PB. Th1 cytokines in oral lichen planus. J Oral Pathol Med. 2003;32(2):77–83.PubMedCrossRef
8.
go back to reference Sugerman PB, Savage NW, Zhou X, Walsh LJ, Bigby M. Oral lichen planus. Clin Dermatol. 2000;18(5):533–9.PubMedCrossRef Sugerman PB, Savage NW, Zhou X, Walsh LJ, Bigby M. Oral lichen planus. Clin Dermatol. 2000;18(5):533–9.PubMedCrossRef
9.
go back to reference Sand L, Jalouli J. Viruses and oral cancer. Is there a link? Microbes and infection. 2014;16(5):371–8. Sand L, Jalouli J. Viruses and oral cancer. Is there a link? Microbes and infection. 2014;16(5):371–8.
10.
go back to reference Speicher DJ, Ramirez-Amador V, Dittmer DP, Webster-Cyriaque J, Goodman MT, Moscicki AB. Viral infections associated with oral cancers and diseases in the context of HIV: a workshop report. Oral Dis. 2016;22:181–92.PubMedPubMedCentralCrossRef Speicher DJ, Ramirez-Amador V, Dittmer DP, Webster-Cyriaque J, Goodman MT, Moscicki AB. Viral infections associated with oral cancers and diseases in the context of HIV: a workshop report. Oral Dis. 2016;22:181–92.PubMedPubMedCentralCrossRef
11.
go back to reference Scully C. Oral squamous cell carcinoma; from an hypothesis about a virus, to concern about possible sexual transmission. Oral Oncol. 2002;38(3):227–34.PubMedCrossRef Scully C. Oral squamous cell carcinoma; from an hypothesis about a virus, to concern about possible sexual transmission. Oral Oncol. 2002;38(3):227–34.PubMedCrossRef
12.
go back to reference Campisi G, Panzarella V, Giuliani M, Lajolo C, Di Fede O, Falaschini S, et al. Human papillomavirus: Its identikit and controversial role in oral oncogenesis, premalignant and malignant lesions. Int J Oncol. 2007;30(4):813–23.PubMed Campisi G, Panzarella V, Giuliani M, Lajolo C, Di Fede O, Falaschini S, et al. Human papillomavirus: Its identikit and controversial role in oral oncogenesis, premalignant and malignant lesions. Int J Oncol. 2007;30(4):813–23.PubMed
13.
go back to reference Andrews E, Seaman WT, Webster-Cyriaque J. Oropharyngeal carcinoma in non-smokers and non-drinkers: a role for HPV. Oral Oncol. 2009;45(6):486–91.PubMedCrossRef Andrews E, Seaman WT, Webster-Cyriaque J. Oropharyngeal carcinoma in non-smokers and non-drinkers: a role for HPV. Oral Oncol. 2009;45(6):486–91.PubMedCrossRef
14.
go back to reference Shimakage M, Horii K, Tempaku A, Kakudo K, Shirasaka T, Sasagawa T. Association of Epstein-Barr virus with oral cancers. Hum Pathol. 2002;33(6):608–14.PubMedCrossRef Shimakage M, Horii K, Tempaku A, Kakudo K, Shirasaka T, Sasagawa T. Association of Epstein-Barr virus with oral cancers. Hum Pathol. 2002;33(6):608–14.PubMedCrossRef
15.
go back to reference Sand LP, Jalouli J, Larsson P-A, Hirsch J-M. 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 Endodontol. 2002;93(5):586–92.CrossRef Sand LP, Jalouli J, Larsson P-A, Hirsch J-M. 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 Endodontol. 2002;93(5):586–92.CrossRef
16.
go back to reference Shamaa AA, Zyada MM, Wagner M, Awad SS, Osman MM, Azeem AAA. The significance of Epstein Barr virus (EBV) & DNA topoisomerase II alpha (DNA-Topo II alpha) immunoreactivity in normal oral mucosa, oral epithelial dysplasia (OED) and oral squamous cell carcinoma (OSCC). Diagn Pathol. 2008;3(1):1–13.CrossRef Shamaa AA, Zyada MM, Wagner M, Awad SS, Osman MM, Azeem AAA. The significance of Epstein Barr virus (EBV) & DNA topoisomerase II alpha (DNA-Topo II alpha) immunoreactivity in normal oral mucosa, oral epithelial dysplasia (OED) and oral squamous cell carcinoma (OSCC). Diagn Pathol. 2008;3(1):1–13.CrossRef
17.
go back to reference Began J, Jiménez Y, Murillo J, Poveda R, Diaz JM, Sanchis J, et al. Epstein-Barr virus in oral proliferative verrucous leukoplakia and squamous cell carcinoma: A preliminary study. Med Oral Patol Oral Y Cirugia Bucal. 2008;13(2):110. Began J, Jiménez Y, Murillo J, Poveda R, Diaz JM, Sanchis J, et al. Epstein-Barr virus in oral proliferative verrucous leukoplakia and squamous cell carcinoma: A preliminary study. Med Oral Patol Oral Y Cirugia Bucal. 2008;13(2):110.
18.
go back to reference Kis A, Fehér E, Gáll T, Tar I, Boda R, Tóth ED, et al. Epstein-Barr virus prevalence in oral squamous cell cancer and in potentially malignant oral disorders in an eastern Hungarian population. Eur J Oral Sci. 2009;117(5):536–40.PubMedCrossRef Kis A, Fehér E, Gáll T, Tar I, Boda R, Tóth ED, et al. Epstein-Barr virus prevalence in oral squamous cell cancer and in potentially malignant oral disorders in an eastern Hungarian population. Eur J Oral Sci. 2009;117(5):536–40.PubMedCrossRef
19.
go back to reference Jiang R, Gu X, Moore-Medlin TN, Nathan C-A, Hutt-Fletcher LM. Oral dysplasia and squamous cell carcinoma: correlation between increased expression of CD21, Epstein-Barr virus and CK19. Oral Oncol. 2012;48(9):836–41.PubMedPubMedCentralCrossRef Jiang R, Gu X, Moore-Medlin TN, Nathan C-A, Hutt-Fletcher LM. Oral dysplasia and squamous cell carcinoma: correlation between increased expression of CD21, Epstein-Barr virus and CK19. Oral Oncol. 2012;48(9):836–41.PubMedPubMedCentralCrossRef
20.
go back to reference Hsieh P-P, Tung C-L, Chan AB-W, Liao J-B, Wang J-S, Tseng H-H, et al. EBV viral load in tumor tissue is an important prognostic indicator for nasal NK/T-cell lymphoma. American journal of clinical pathology. 2007;128(4):579–84. Hsieh P-P, Tung C-L, Chan AB-W, Liao J-B, Wang J-S, Tseng H-H, et al. EBV viral load in tumor tissue is an important prognostic indicator for nasal NK/T-cell lymphoma. American journal of clinical pathology. 2007;128(4):579–84.
21.
go back to reference Shuda M, Arora R, Kwun HJ, Feng H, Sarid R, Fernández‐Figueras MT, et al. Human Merkel cell polyomavirus infection I. MCV T antigen expression in Merkel cell carcinoma, lymphoid tissues and lymphoid tumors. International journal of cancer. 2009;125(6):1243–9. Shuda M, Arora R, Kwun HJ, Feng H, Sarid R, Fernández‐Figueras MT, et al. Human Merkel cell polyomavirus infection I. MCV T antigen expression in Merkel cell carcinoma, lymphoid tissues and lymphoid tumors. International journal of cancer. 2009;125(6):1243–9.
22.
23.
go back to reference Hui KF, Chan TF, Yang W, Shen JJ, Lam KP, Kwok H, et al. High risk Epstein-Barr virus variants characterized by distinct polymorphisms in the EBER locus are strongly associated with nasopharyngeal carcinoma. Int J Cancer. 2019;144(12):3031–42.PubMedCrossRef Hui KF, Chan TF, Yang W, Shen JJ, Lam KP, Kwok H, et al. High risk Epstein-Barr virus variants characterized by distinct polymorphisms in the EBER locus are strongly associated with nasopharyngeal carcinoma. Int J Cancer. 2019;144(12):3031–42.PubMedCrossRef
24.
go back to reference Palser AL, Grayson NE, White RE, Corton C, Correia S, Ba abdullah MM, et al. Genome diversity of Epstein-Barr virus from multiple tumor types and normal infection. J Virol. 2015;89(10):5222–37. Palser AL, Grayson NE, White RE, Corton C, Correia S, Ba abdullah MM, et al. Genome diversity of Epstein-Barr virus from multiple tumor types and normal infection. J Virol. 2015;89(10):5222–37.
25.
go back to reference Yahyapour Y, Shamsi-Shahrabadi M, Mahmoudi M, Siadati S, Shahryar SS, Shokri-Shirvani J, et al. Evaluation of human papilloma virus infection in patients with esophageal squamous cell carcinoma from the Caspian Sea area, north of Iran. Asian Pac J Cancer Prev. 2012;13(4):1261–6.PubMedCrossRef Yahyapour Y, Shamsi-Shahrabadi M, Mahmoudi M, Siadati S, Shahryar SS, Shokri-Shirvani J, et al. Evaluation of human papilloma virus infection in patients with esophageal squamous cell carcinoma from the Caspian Sea area, north of Iran. Asian Pac J Cancer Prev. 2012;13(4):1261–6.PubMedCrossRef
26.
go back to reference Ling PD, Vilchez RA, Keitel WA, Poston DG, Peng RS, White ZS, et al. Epstein-Barr virus DNA loads in adult human immunodeficiency virus type 1-infected patients receiving highly active antiretroviral therapy. Clin Infect Dis. 2003;37(9):1244–9.PubMedCrossRef Ling PD, Vilchez RA, Keitel WA, Poston DG, Peng RS, White ZS, et al. Epstein-Barr virus DNA loads in adult human immunodeficiency virus type 1-infected patients receiving highly active antiretroviral therapy. Clin Infect Dis. 2003;37(9):1244–9.PubMedCrossRef
27.
go back to reference Sadeghi F, Salehi-Vaziri M, Ghodsi SM, Alizadeh A, Bokharaei-Salim F, Saroukalaei ST, et al. Prevalence of JC polyomavirus large T antigen sequences among Iranian patients with central nervous system tumors. Adv Virol. 2015;160(1):61–8. Sadeghi F, Salehi-Vaziri M, Ghodsi SM, Alizadeh A, Bokharaei-Salim F, Saroukalaei ST, et al. Prevalence of JC polyomavirus large T antigen sequences among Iranian patients with central nervous system tumors. Adv Virol. 2015;160(1):61–8.
28.
go back to reference Lin J-C, Lin S-C, De BK, Chan W-P, Evatt BL. Precision of genotyping of Epstein-Barr virus by polymerase chain reaction using three gene loci (EBNA-2, EBNA-3C, and EBER): predominance of type A virus associated with Hodgkin’s disease. Blood. 1993;81(12):3372–81.PubMedCrossRef Lin J-C, Lin S-C, De BK, Chan W-P, Evatt BL. Precision of genotyping of Epstein-Barr virus by polymerase chain reaction using three gene loci (EBNA-2, EBNA-3C, and EBER): predominance of type A virus associated with Hodgkin’s disease. Blood. 1993;81(12):3372–81.PubMedCrossRef
29.
go back to reference Arrand JR, Young L, Tugwood J. Two families of sequences in the small RNA-encoding region of Epstein-Barr virus (EBV) correlate with EBV types A and B. J Virol. 1989;63(2):983–6.PubMedPubMedCentralCrossRef Arrand JR, Young L, Tugwood J. Two families of sequences in the small RNA-encoding region of Epstein-Barr virus (EBV) correlate with EBV types A and B. J Virol. 1989;63(2):983–6.PubMedPubMedCentralCrossRef
30.
go back to reference Dhanuthai K, Rojanawatsirivej S, Thosaporn W, Kintarak S, Subarnbhesaj A, Darling M, et al. Oral cancer: A multicenter study. Medicina oral, patologia oral y cirugia bucal. 2018;23(1):e23. Dhanuthai K, Rojanawatsirivej S, Thosaporn W, Kintarak S, Subarnbhesaj A, Darling M, et al. Oral cancer: A multicenter study. Medicina oral, patologia oral y cirugia bucal. 2018;23(1):e23.
31.
go back to reference Orbak R, Bayraktar C, Kavrut F, Gündogdu C. Poor oral hygiene and dental trauma as the precipitating factors of squamous cell carcinoma. Oral Oncol Extra. 2005;41(6):109–13.CrossRef Orbak R, Bayraktar C, Kavrut F, Gündogdu C. Poor oral hygiene and dental trauma as the precipitating factors of squamous cell carcinoma. Oral Oncol Extra. 2005;41(6):109–13.CrossRef
32.
go back to reference Kobayashi I, Shima K, Saito I, Kiyoshima T, Matsuo K, Ozeki S, et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinoma. J Pathol. 1999;189(1):34–9.PubMedCrossRef Kobayashi I, Shima K, Saito I, Kiyoshima T, Matsuo K, Ozeki S, et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinoma. J Pathol. 1999;189(1):34–9.PubMedCrossRef
33.
go back to reference Gonzalez-Moles M, Gutierrez J, Rodriguez M, Ruiz-Avila I, Rodriguez-Archilla A. Epstein-Barr virus latent membrane protein-1 (LMP-1) expression in oral squamous cell carcinoma. Laryngoscope. 2002;112(3):482–7.PubMedCrossRef Gonzalez-Moles M, Gutierrez J, Rodriguez M, Ruiz-Avila I, Rodriguez-Archilla A. Epstein-Barr virus latent membrane protein-1 (LMP-1) expression in oral squamous cell carcinoma. Laryngoscope. 2002;112(3):482–7.PubMedCrossRef
34.
go back to reference D’Costa J, Saranath D, Sanghvi V, Mehta AR. Epstein-Barr virus in tobacco-induced oral cancers and oral lesions in patients from India. J Oral Pathol Med. 1998;27(2):78–82.PubMedCrossRef D’Costa J, Saranath D, Sanghvi V, Mehta AR. Epstein-Barr virus in tobacco-induced oral cancers and oral lesions in patients from India. J Oral Pathol Med. 1998;27(2):78–82.PubMedCrossRef
35.
go back to reference Hermann R, Füzesi L, Pradier O, Christiansen H, Schmidberger H. Presence of human papillomavirus-18 and Epstein–Barr virus in a squamous cell carcinoma of the tongue in a 20-year-old patient. Case report and review of the current literature. Cancer/Radiothérapie. 2004;8(4):262–5. Hermann R, Füzesi L, Pradier O, Christiansen H, Schmidberger H. Presence of human papillomavirus-18 and Epstein–Barr virus in a squamous cell carcinoma of the tongue in a 20-year-old patient. Case report and review of the current literature. Cancer/Radiothérapie. 2004;8(4):262–5.
36.
go back to reference Tsuhako K, Nakazato I, Miyagi J, Iwamasa T, Arasaki A, Hiratsuka H, et al. Comparative study of oral squamous cell carcinoma in Okinawa, Southern Japan and Sapporo in Hokkaido, Northern Japan; with special reference to human papillomavirus and Epstein-Barr virus infection. J Oral Pathol Med. 2000;29(2):70–9.PubMedCrossRef Tsuhako K, Nakazato I, Miyagi J, Iwamasa T, Arasaki A, Hiratsuka H, et al. Comparative study of oral squamous cell carcinoma in Okinawa, Southern Japan and Sapporo in Hokkaido, Northern Japan; with special reference to human papillomavirus and Epstein-Barr virus infection. J Oral Pathol Med. 2000;29(2):70–9.PubMedCrossRef
37.
go back to reference Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt’s lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J Virol. 1994;68(9):6069–73.PubMedPubMedCentralCrossRef Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt’s lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J Virol. 1994;68(9):6069–73.PubMedPubMedCentralCrossRef
38.
go back to reference Horiuchi K, Mishima K, Ichijima K, Sugimura M, Ishida T, Kirita T. Epstein-Barr virus in the proliferative diseases of squamous epithelium in the oral cavity. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 1995;79(1):57–63.CrossRef Horiuchi K, Mishima K, Ichijima K, Sugimura M, Ishida T, Kirita T. Epstein-Barr virus in the proliferative diseases of squamous epithelium in the oral cavity. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 1995;79(1):57–63.CrossRef
39.
go back to reference Cruz I, Van den Brule A, Steenbergen R, Snijders P, Meijer C, Walboomers J, et al. Prevalence of Epstein–Barr virus in oral squamous cell carcinomas, premalignant lesions and normal mucosa—a study using the polymerase chain reaction. Oral Oncol. 1997;33(3):182–8.PubMedCrossRef Cruz I, Van den Brule A, Steenbergen R, Snijders P, Meijer C, Walboomers J, et al. Prevalence of Epstein–Barr virus in oral squamous cell carcinomas, premalignant lesions and normal mucosa—a study using the polymerase chain reaction. Oral Oncol. 1997;33(3):182–8.PubMedCrossRef
40.
go back to reference Tsang NM, Chang KP, Lin SY, Hao SP, Tseng CK, Kuo Tt, et al. Detection of Epstein‐Barr Virus–Derived Latent Membrane Protein‐1 Gene in Various Head and Neck Cancers: Is It Specific for Nasopharyngeal Carcinoma? The Laryngoscope. 2003;113(6):1050–4. Tsang NM, Chang KP, Lin SY, Hao SP, Tseng CK, Kuo Tt, et al. Detection of Epstein‐Barr Virus–Derived Latent Membrane Protein‐1 Gene in Various Head and Neck Cancers: Is It Specific for Nasopharyngeal Carcinoma? The Laryngoscope. 2003;113(6):1050–4.
41.
go back to reference Prathyusha MM, Kattappagari KK, Chowdary D, Shekar PC, Alivelu D, Reddy BVR. A study on association of epstein barr virus in oral squamous cell carcinoma using polymerase chain reaction technique. J Dr NTR Univ Health Sci. 2019;8(4):233.CrossRef Prathyusha MM, Kattappagari KK, Chowdary D, Shekar PC, Alivelu D, Reddy BVR. A study on association of epstein barr virus in oral squamous cell carcinoma using polymerase chain reaction technique. J Dr NTR Univ Health Sci. 2019;8(4):233.CrossRef
42.
go back to reference Iamaroon A, Khemaleelakul U, Pongsiriwet S, Pintong J. Co-expression of p53 and Ki67 and lack of EBV expression in oral squamous cell carcinoma. J Oral Pathol Med. 2004;33(1):30–6.PubMedCrossRef Iamaroon A, Khemaleelakul U, Pongsiriwet S, Pintong J. Co-expression of p53 and Ki67 and lack of EBV expression in oral squamous cell carcinoma. J Oral Pathol Med. 2004;33(1):30–6.PubMedCrossRef
43.
go back to reference Kerishnan JP, Mah MK, Mohd Fawzi NA, Ramanathan A, Lim GS, Abdul Aziz A, et al. The association between Epstein-Barr virus (EBV) Past Infection with the risk of oral squamous cell carcinoma (OSCC). Sains Malaysiana. 2019;48(9):1969–74.CrossRef Kerishnan JP, Mah MK, Mohd Fawzi NA, Ramanathan A, Lim GS, Abdul Aziz A, et al. The association between Epstein-Barr virus (EBV) Past Infection with the risk of oral squamous cell carcinoma (OSCC). Sains Malaysiana. 2019;48(9):1969–74.CrossRef
44.
go back to reference Maeda T, Hiranuma H, Matsumura S, Furukawa S, Fuchihata H. Epstein-Barr virus infection and response to radiotherapy in squamous cell carcinoma of the oral cavity. Cancer Lett. 1998;125(1–2):25–30.PubMedCrossRef Maeda T, Hiranuma H, Matsumura S, Furukawa S, Fuchihata H. Epstein-Barr virus infection and response to radiotherapy in squamous cell carcinoma of the oral cavity. Cancer Lett. 1998;125(1–2):25–30.PubMedCrossRef
45.
go back to reference Saravani S, Miri-Moghaddam E, Sanadgol N, Kadeh H, Nazeri MR. Human herpesvirus-6 and Epstein-Barr virus infections at different histopathological grades of oral squamous cell carcinomas. Int J Prev Med. 2014;5(10):1231.PubMedPubMedCentral Saravani S, Miri-Moghaddam E, Sanadgol N, Kadeh H, Nazeri MR. Human herpesvirus-6 and Epstein-Barr virus infections at different histopathological grades of oral squamous cell carcinomas. Int J Prev Med. 2014;5(10):1231.PubMedPubMedCentral
46.
go back to reference Goldenberg D, Benoit NE, Begum S, Westra WH, Cohen Y, Koch WM, et al. Epstein-Barr virus in head and neck cancer assessed by quantitative polymerase chain reaction. Laryngoscope. 2004;114(6):1027–31.PubMedCrossRef Goldenberg D, Benoit NE, Begum S, Westra WH, Cohen Y, Koch WM, et al. Epstein-Barr virus in head and neck cancer assessed by quantitative polymerase chain reaction. Laryngoscope. 2004;114(6):1027–31.PubMedCrossRef
47.
go back to reference Bagan JV, Jiménez Y, Murillo J, Poveda R, Díaz JM, Gavaldá C, et al. Epstein-Barr virus in oral proliferative verrucous leukoplakia and squamous cell carcinoma: A preliminary study. Med Oral Patol Oral Cir Bucal. 2008;13(2):E110–3.PubMed Bagan JV, Jiménez Y, Murillo J, Poveda R, Díaz JM, Gavaldá C, et al. Epstein-Barr virus in oral proliferative verrucous leukoplakia and squamous cell carcinoma: A preliminary study. Med Oral Patol Oral Cir Bucal. 2008;13(2):E110–3.PubMed
48.
go back to reference Cruz I, Van den Brule AJ, Steenbergen RD, Snijders PJ, Meijer CJ, Walboomers JM, et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinomas, premalignant lesions and normal mucosa–a study using the polymerase chain reaction. Oral Oncol. 1997;33(3):182–8.PubMedCrossRef Cruz I, Van den Brule AJ, Steenbergen RD, Snijders PJ, Meijer CJ, Walboomers JM, et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinomas, premalignant lesions and normal mucosa–a study using the polymerase chain reaction. Oral Oncol. 1997;33(3):182–8.PubMedCrossRef
49.
go back to reference Jiang R, Ekshyyan O, Moore-Medlin T, Rong X, Nathan S, Gu X, et al. Association between human papilloma virus/Epstein-Barr virus coinfection and oral carcinogenesis. J Oral Pathol Med. 2015;44(1):28–36.PubMedCrossRef Jiang R, Ekshyyan O, Moore-Medlin T, Rong X, Nathan S, Gu X, et al. Association between human papilloma virus/Epstein-Barr virus coinfection and oral carcinogenesis. J Oral Pathol Med. 2015;44(1):28–36.PubMedCrossRef
50.
go back to reference Sand LP, Jalouli J, Larsson PA, 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. 2002;93(5):586–92.PubMedCrossRef Sand LP, Jalouli J, Larsson PA, 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. 2002;93(5):586–92.PubMedCrossRef
51.
go back to reference Wang Y, Zhang X, Chao Y, Jia Y, Xing X, Luo B. New variations of Epstein-Barr virus-encoded small RNA genes in nasopharyngeal carcinomas, gastric carcinomas, and healthy donors in northern China. J Med Virol. 2010;82(5):829–36.PubMedCrossRef Wang Y, Zhang X, Chao Y, Jia Y, Xing X, Luo B. New variations of Epstein-Barr virus-encoded small RNA genes in nasopharyngeal carcinomas, gastric carcinomas, and healthy donors in northern China. J Med Virol. 2010;82(5):829–36.PubMedCrossRef
52.
go back to reference Schuster V, Ott G, Seidenspinner S, Kreth HW. Common Epstein-Barr virus (EBV) type-1 variant strains in both malignant and benign EBV-associated disorders. 1996. Schuster V, Ott G, Seidenspinner S, Kreth HW. Common Epstein-Barr virus (EBV) type-1 variant strains in both malignant and benign EBV-associated disorders. 1996.
53.
go back to reference Xiaoshi Z, Linjie Z, Ruhua Z, Haiqiang M, Jianjing C, Yixin Z. Relationship between polymorphism of Epstein-Barrvirus-encoded small RNAs and nasopharyngeal carcinomas. J Pract Oncol. 2001;16(5):301–3. Xiaoshi Z, Linjie Z, Ruhua Z, Haiqiang M, Jianjing C, Yixin Z. Relationship between polymorphism of Epstein-Barrvirus-encoded small RNAs and nasopharyngeal carcinomas. J Pract Oncol. 2001;16(5):301–3.
54.
go back to reference Dolan A, Addison C, Gatherer D, Davison AJ, McGeoch DJ. The genome of Epstein-Barr virus type 2 strain AG876. Virology. 2006;350(1):164–70.PubMedCrossRef Dolan A, Addison C, Gatherer D, Davison AJ, McGeoch DJ. The genome of Epstein-Barr virus type 2 strain AG876. Virology. 2006;350(1):164–70.PubMedCrossRef
55.
go back to reference Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10(3):512–26.PubMed Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10(3):512–26.PubMed
Metadata
Title
Detection of Epstein-Barr virus encoded small RNA genes in oral squamous cell carcinoma and non-cancerous oral cavity samples
Authors
Arghavan Zebardast
Yousef Yahyapour
Maryam Seyed Majidi
Mohammad Chehrazi
Farzin Sadeghi
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2021
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-021-01867-8

Other articles of this Issue 1/2021

BMC Oral Health 1/2021 Go to the issue