Koumpouli Alexandra, Karavida Paulina, Zisis Vasileios, Poulopoulos Athanasios, Andreadis Dimitrios
Aristotle University of Thessaloniki, Faculty of Health Sciences, School of Dentistry, Department of Oral Medicine/Pathology, Thessaloniki, Greece
Abstract
Epstein Barr virus (EBV) is the first virus identified to possess the capacity to induce various benign and malignant conditions. These conditions encompass asymptomatic persistent infection, self-limited disease in individuals with a competent immune system, and the propensity to initiate different tumors formation (oncogenesis) even head and neck cancer. Notably, EBV may interact with other viruses including human papillomavirus (HPV) especially in immunosuppressed patients, leading to a synergistic effect. The objective of this study is to conduct a comprehensive literature review on the Epstein-Barr virus (EBV), focusing on its life cycle within the human host, the pathogenic mechanisms associated with the virus, the specific types of head and neck cancers in which EBV is implicated, and the interactions between EBV and other viruses in immunosuppressed individuals. Epstein-Barr virus (EBV) remains in most cases, asymptomatic or leads to the development of infectious mononucleosis. Moreover, it plays a significant role in the development of cancer, particularly in individuals under immunosuppression. The viral infection typically persists within the host organism in either a dormant or lytic state. The research also addresses the topic of chronic activated Epstein-Barr virus (EBV) syndrome, exploring its interactions with other pathogenic viruses. In addition to presenting oral manifestations in the form of infectious mononucleosis, the Epstein-Barr virus (EBV) is linked to the occurrence of nasopharyngeal carcinoma, Hodgkin and Non-Hodgkin lymphomas in the head and neck region. Furthermore, EBV is associated with the development of hairy leukoplakia in individuals with weakened immune systems due to HIV. Overall, EBV may play a role in the etiology and pathogenesis of oral squamous epithelium carcinoma either independently or in conjunction with human papillomavirus (HPV). The manifold role of EBV necessitates the accurate diagnosis of new cases and the vigilant monitoring of the patients in order to avoid or at least delay the long term repercussions on the patients’ health and quality of life.
Keywords: HPV; EBV; LMP protein; nasopharyngeal carcinoma; Hodgkin lymphoma; Non-Hodgkin lymphoma
Reference
Abdelrahim, L.M., Peh, S.C., Kallarakkal, T.G. (2018) Epstein-Barr virus infection in B-cell Non-Hodgkin’s lymphomas of the oral and Maxillofacial Region: Is there any evidence?. Malays J Pathol, 40 (1): 49-56
Abdullah, B., Alias, A., Hassan, S. (2009) Challenges in the management of nasopharyngeal carcinoma: A review. Malays J Med Sci, 16 (4): 50-54
Adham, M., Kurniawan, A.N., Muhtadi, A.I., Roezin, A., Hermani, B., Gondhowiardjo, S., et al. (2012) Nasopharyngeal carcinoma in Indonesia: Epidemiology, incidence, signs, and symptoms at presentation. Chin J Cancer, 31 (4): 185-196, Epub 2012 Feb 7
Aguayo, F., Boccardo, E., Corvalán, A., Calaf, G.M., Blanco, R. (2021) Interplay between Epstein-Barr virus infection and environmental xenobiotic exposure in cancer. Infect Agent Cancer, 16 (1): 50
Ahmed, N., Abusalah, M., Farzand, A., Absar, M., Yusof, N.Y., Rabaan, A.A., et al. (2022) Updates on Epstein-Barr Virus (EBV)-Associated Nasopharyngeal Carcinoma: Emphasis on the Latent gene products of EBV. Medicina (Kaunas), 59 (1): 2
Arai, A. (2019) Advances in the study of chronic active Epstein-Barr virus infection: Clinical features under the 2016 WHO classification and mechanisms of development. Frontiers in Pediatrics, 7: 14-14
Arai, A. (2021) Chronic active Epstein-Barr virus infection: The elucidation of the pathophysiology and the development of therapeutic methods. Microorganisms, 9(1): 180-180
Argirion, I., Zarins, K.R., Suwanrungruang, K., Pongnikorn, D., Chitapanarux, I., Sriplung, H. (2020) Subtype specific Nasopharyngeal carcinoma incidence and survival trends: differences between endemic and Nonendemic populations. Asian Pac J Cancer Prev, 21(11): 3291-3299
Ayee, R., Ofori, M.E.O., Wright, E., Quaye, O. (2020) Epstein Barr virus associated lymphomas and Epithelia cancers in humans. J Cancer, 11 (7): 1737-1750
Azad, F.J., Delavarian, Z., Hatami, M., Rahimi, H., Abdolvahedi, M.R. (2017) Extranodal NK/T Cell Lymphoma with Destruction of the Uvulae: A case report. Iran J Otorhinolaryngol, 29 (91): 101-108
Banko, A., Miljanovic, D., Lazarevic, I., Cirkovic, A. (2023) A systematic review of Epstein-Barr virus latent membrane Protein 1 (lmp1) gene variants in Nasopharyngeal carcinoma. Pathogens, 10(8): 1057-1057
Bertrand, K.A., Birmann, B.M., Chang, E.T., Spiegelman, D., Aster, J.C., Zhang, S.M., Laden, F. (2010) A prospective study of Epstein-Barr virus antibodies and risk of non-Hodgkin lymphoma. Blood, 116(18): 3547-3553
Biko, D.M., Anupindi, S.A., Hernandez, A., Kersun, L., Bellah, R. (2009) Childhood Burkitt lymphoma: Abdominal and pelvic imaging findings. AJR Am J Roentgenol, 192 (5): 1304-1315
Brady, G., Macarthur, G.J., Farrell, P.J. (2008) Epstein-Barr virus and Burkitt lymphoma. Postgrad Med J, 84 (993): 372-377
Cairo, M.S., Sposto, R., Perkins, S.L., Meadows, A.T., Hoover-Regan, M.L., Anderson, J.R., et al. (2003) Burkitt’s and Burkitt-like lymphoma in children and adolescents: A review of the Children’s Cancer Group experience. Br J Haematol, 120 (4): 660-670
Calabretta, E., D’amore, F., Carlo-Stella, C. (2019) Immune and inflammatory cells of the tumor microenvironment represent novel therapeutic targets in classical Hodgkin Lymphoma. International Journal of Molecular Sciences, 20(21): 5503-5503
Castillo, J.J., Beltran, B.E., Miranda, R.N., Young, K.H., Chavez, J.C., Sotomayor, E.M. (2016) EBV-positive diffuse large B-cell lymphoma of the elderly: 2016 update on diagnosis, risk-stratification, and management. American Journal of Hematology, 91(5): 529-537
Castillo, J.J., Beltran, B.E., Miranda, R.N., Paydas, S., Winer, E.S., Butera, J.N. (2011) Epstein-barr virus-positive diffuse large B-cell lymphoma of the elderly: what we know so far. Oncologist, 16(1): 87-96
Chabay, P. (2021) Advances in the Pathogenesis of EBVAssociated Diffuse Large B Cell Lymphoma. Cancers (Basel), 133(11): 2717-2717
Chan, A.S.C., To, K.F., Lo, K.W., Ding, M., Li, X., Johnson, P., et al. (2002) Frequent chromosome 9p losses in histologically normal nasopharyngeal epithelia from southern Chinese. Int J Cancer, 102 (3): 300-303
Chan, J.K.C. (2017) Virus-associated neoplasms of the nasopharynx and sinonasal tract: Diagnostic problems. Mod Pathol, 30 (s1): S68-S83
Chen, J. (2012) Roles of the PI3K/Akt pathway in Epstein-Barr virus-induced cancers and therapeutic implications. World Journal of Virology, 1 (6): 154-161
Chen, Z., Liu, W., Zhang, W., Ye, Y., Guan, P., Gao, L., et al. (2019) Chronic active Epstein-Barr virus infection of T/NK-Cell type mimicking classic Hodgkin Lymphoma: Clinicopathologic and genetic features of 8 cases supporting a variant with ‘Hodgkin/Reed-Sternberglike’ cells of NK phenotype. Am J Surg Pathol, 43 (12): 1611-1621
Clarke, C.A., Morton, L.M., Lynch, C., Pfeiffer, R.M., Hall, E.C., Gibson, T.M., Weisenburger, D.D., Martínez-Maza, O., Hussain, S.K., Yang, J., Chang, E.T., Engels, E.A. (2013) Risk of lymphoma subtypes after solid organ transplantation in the United States. British Journal of Cancer, 109(1): 280-288
1
Dalla-Favera, R., Bregni, M., Erikson, J., Patterson, D., Gallo, R.C., Croce, C.M. (1982) Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci USA, 79 (24): 7824-7827
Dawson, C.W., Tramountanis, G., Eliopoulos, A.G., Young, L.S. (2003) Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J Biol Chem, 278(6): 3694-3704
de la Cruz-Merino, L., Lejeune, M., Fernández, N.E., Carrasco, H.F., López, G.A., Vacas, I.A., et al. (2012) Role of immune escape mechanisms in Hodgkin’s lymphoma development and progression: A whole new world with therapeutic implications. Clin Dev Immunol, 756353-756353
de Melo, S.J., Pinheiro-Silva, R., Dhyani, A., Pontes, G.S. (2020) Cytomegalovirus and Epstein-Barr Infections: Prevalence and Impact on Patients with Hematological Diseases. Biomed Res Int, 2020 : 1627824
Dorothea, M., Xie, J., Yiu, S.P.T., Chiang, A.K.S. (2023) Contribution of Epstein-Barr virus Lytic proteins to cancer hallmarks and implications from other Oncoviruses. Cancers (Basel), 15 (7): 2120
Dozzo, M., Carobolante, F., Donisi, P.M., Scattolin, A., Maino, E., Sancetta, R., et al. (2017) Burkitt lymphoma in adolescents and young adults: Management challenges. Adolesc Health Med Ther, 8: 11-29
Dunmire, S.K., Verghese, P.S., Balfour, H.H. (2018) Primary Epstein-Barr virus infection. J Clin Virol, 102: 84-92
Fox, C.P., Civallero, M., Ko, Y.H., Manni, M., Skrypets, T., Pileri, S., et al. (2020) Survival outcomes of patients with extranodal natural-killer T-cell lymphoma: A prospective cohort study from the international T-cell Project. Lancet Haematol, 7 (4): e284-294
Fujiwara, S., Nakamura, H. (2020) Chronic active Epstein-Barr virus infection: Is it immunodeficiency, malignancy, or both?. Cancers (Basel), 12 (11): 3202
Gandhi, M.K., Tellam, J.T., Khanna, R. (2004) Epstein-Barr virus-associated Hodgkin’s lymphoma. Br J Haematol, 125 (3): 267-281
Gequelin, L.C.F., Riediger, I.N., Nakatani, S.M., Biondo, A.W., Bonfim, C.M. (2011) Epstein-Barr virus: general factors, virus-related diseases and measurement of viral load after transplant. Rev Bras Hematol Hemoter, 33 (5): 383-388
Gessese, T., Asrie, F., Mulatie, Z. (2023) Human Immunodeficiency Virus Related Non-Hodgkin’s Lymphoma. Blood Lymphat Cancer, 13: 13-24
Giunco, S., Celeghin, A., Gianesin, K., Dolcetti, R., Indraccolo, S., de Rossi, A. (2015) Cross talk between EBV and telomerase: The role of TERT and NOTCH2 in the switch of latent/lytic cycle of the virus. Cell Death Dis, 6 (5): e1774
Giunco, S., Petrara, M.R., Zangrossi, M., Celeghin, A., de Rossi, A. (2018) Extra-telomeric functions of telomerase in the pathogenesis of Epstein-Barr virus-driven B-cell malignancies and potential therapeutic implications. Infect Agent Cancer, 13: 14
Green, M., Michaels, M.G. (2013) Epstein-Barr virus infection and posttransplant lymphoproliferative disorder. American Journal of Transplantation, 13 (3): 41-54
Guidry, J.T., Birdwell, C.E., Scott, R.S. (2018) Epstein-Barr virus in the pathogenesis of oral cancers. Oral Diseases, 24(4): 497-508
1
Gupta, N., Gupta, R., Acharya, A.K., Patthi, B., Goud, V., Reddy, S., Garg, A., Singla, A. (2016) Changing trends in oral cancer: A global scenario. Nepal Journal of Epidemiology, 6(4): 613-619
Hatton, O.L., Harris-Arnold, A., Schaffert, S., Krams, S.M., Martinez, O.M. (2014) The interplay between Epstein Barr virus and b lymphocytes: Implications for infection, immunity, and disease. Immunol Res, 58(2-3): 268-276
Hau, P.M., Lung, H.L., Wu, M., Tsang, C.M., Wong, K.L., Mak, N.K., et al. (2020) Targeting Epstein-Barr virus in Nasopharyngeal carcinoma. Front Oncol, 10 : 600
Huang, H., Liu, Z.L., Zeng, H., Zhang, S.H., Huang, C.S., Xu, H.Y., et al. (2015) Clinicopathological study of sporadic Burkitt lymphoma in children. Chin Med J (Engl), 128 (4): 510-514
Humme, S., Reisbach, G., Feederle, R., Delecluse, H.J., Bousset, K., Hammerschmidt, W., et al. (2003) The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold. Proc Natl Acad Sci USA, 100 (19): 10989-10994
Ichi, K.J., Ito, Y., Ohshima, K., Yamada, M., Kataoka, S., Muramatsu, H., et al. (2023) Updated guidelines for chronic active Epstein-Barr virus disease. Int J Hematol, 118 (5): 568-576
Iwakiri, D. (2014) Epstein-Barr Virus-Encoded RNAs: Key molecules in viral Pathogenesis. Cancers (Basel), 6 (3): 1615-1630
Jain, A., Chia, W.K., Toh, H.C. (2016) Immunotherapy for nasopharyngeal cancer: A review. Chin Clin Oncol, 5 (2): 22
Jia, Y., Byers, J., Mason, H., Qing, X. (2019) Educational Case: Extranodal NK/T-Cell Lymphoma, Nasal Type. Academic Pathology, 6: 2374289519893083
Jiang, N., Dai, Q., Su, X., Fu, J., Feng, X., Peng, J. (2020) Role of PI3K/AKT pathway in cancer: the framework of malignant behavior. Mol Biol Rep, 47(6): 4587-4629
Jicman, S.D., Niculet, E., Lungu, M., Onisor, C., Rebegea, L., Vesa, D., Bezman, L., Bujoreanu, F., Sarbu, M., Mihailov, R., Fotea, S., Tatu, A. (2022) Nasopharyngeal carcinoma: A new synthesis of literature data (Review). Experimental and Therapeutic Medicine, 23(2): 35069817-35069817
Johnson, D.E., Burtness, B., Leemans, C.R., Lui, V., Bauman, J.E., Grandis, J.R. (2023) Head and neck squamous cell carcinoma. Nat Rev Dis Primers, 6 (1): 92
Johnston, W.T., Mutalima, N., Sun, D., Emmanuel, B., Bhatia, K., Aka, P., et al. (2014) Relationship between Plasmodium falciparum malaria prevalence, genetic diversity and endemic Burkitt lymphoma in Malawi. Sci Rep, 4 : 3741
Khammissa, R., Fourie, J., Chandran, R., Lemmer, J., Feller, L. (2016) Epstein-Barr virus and its association with oral hairy Leukoplakia: A short review. Int J Dent, 2016 : 4941783
Kimura, H., Kawada, J.I., Ito, Y. (2013) Epstein-barr virusassociated lymphoid malignancies: The expanding spectrum of hematopoietic neoplasms. Nagoya J Med Sci, 75 (3-4): 169-79
Kimura, H., Cohen, J.I. (2017) Chronic active Epstein-Barr virus disease. Front Immunol, 8 : 1867
Kreuter, A., Wieland, U. (2011) Oral hairy leukoplakia: A clinical indicator of immunosuppression. CMAJ, 183(8): 932-932
Lanoy, E., Rosenberg, P.S., Fily, F., Lascaux, A.S., Martinez, V., Partisani, M., et al. (2011) HIV-associated Hodgkin lymphoma during the first months on combination antiretroviral therapy. Blood, 118(1): 44-49
Lee, T.H., Ko, Y.H. (2016) Chronic active EBV infection: The experience of the Samsung Medical Center in South Korea. Bol Med Hosp Infant Mex, 73 (1): 10-17
Li, J., Chen, S., Peng, S., Liu, Y., Xing, S., He, X., et al. (2018) Prognostic nomogram for patients with Nasopharyngeal Carcinoma incorporating hematological biomarkers and clinical characteristics. Int J Biol Sci, 14 (5): 549-556
Linch, D.C. (2012) Burkitt lymphoma in adults. Br J Haematol, 156(6): 693-703
Lino, C., Ghosh, S. (2019) Epstein-Barr virus in inborn immunodeficiency-more than infection. Cancers (Basel), 13: 4752-4752
Liu, C.Y., Chen, B.J., Chuang, S.S. (2022) Primary effusion Lymphoma: A timely review on the association with HIV, hhv8, and EBV. Diagnostics (Basel), 12(3): 713-713
Liu, W., Yang, Y., Qi, S., Wang, Y., He, X., Zhang, L., et al. (2021) Treatment, survival, and prognosis of advanced-stage natural killer/t-cell Lymphoma: An analysis from the China Lymphoma collaborative group. Front Oncol, 10: 583050-583050
Liu, X., Cohen, J.I. (2015) Epstein-Barr Virus (EBV) Tegument Protein BGLF2 Promotes EBV Reactivation through Activation of the p38 Mitogen-Activated protein kinase. J Virol, 90 (2): 1129-1138
1
Lizasa, H., Nanbo, A., Nishikawa, J., Jinushi, M., Yoshiyama, H. (2012) Epstein-Barr Virus (EBV)-associated Gastric Carcinoma. Viruses, 4(12): 3420-39
Lo, A.K.F., Dawson, C.W., Lung, H.L., Wong, K.L., Young, L.S. (2021) The Role of EBV-Encoded LMP1 in the NPC tumor microenvironment: From Function to Therapy. Front Oncol, 11: 640207
Lo, K.W., Huang, D.P. (2002) Genetic and epigenetic changes in nasopharyngeal carcinoma. Semin Cancer Biol, 12 (6): 451-462
Louten, J. (2016) Virus replication. Essential human virology. 49-70
Luo, Y., Liu, Y., Wang, C., Gan, R. (2021) Signaling pathways of EBV-induced oncogenesis. Cancer Cell Int, 21(1): 93-93
Martinez, O.M., Krams, S.M. (2017) The Immune response to Epstein Barr Virus and Implications for posttransplant Lymphoproliferative Disorder. Transplantation, 101 (9): 2009-2016
Michelow, P., Wright, C., Pantanowitz, L. (2012) A review of the cytomorphology of Epstein-Barr virusassociated malignancies. Acta Cytol, 56(1): 1-14
Milani, C., Stadler, C., da Silva, G.L., Milani, P. (2022) Non-Hodgkin lymphoma of a palate: A case report of a highly destructive lesion. J Oral Maxillofac Pathol, 26 (2): 289-290
Molesworth, S.J., Lake, C.M., Borza, C.M., Turk, S.M., Hutt-Fletcher, L.M. (2000) Epstein-Barr virus gH is essential for penetration of B cells but also plays A role in attachment of virus to epithelial cells. J Virol, 74 (14): 6324-6332
Molyneux, E.M., Rochford, R., Griffin, B., Newton, R., Jackson, G., Menon, G., et al. (2012) Burkitt’s lymphoma. Lancet, 379 (9822): 1234-1244
Morales-Sánchez, A., Fuentes-Pananá, E.M. (2014) Human viruses and cancer. Viruses, 6 (10): 4047-4079
Morris, M.A. (2020) Cancer-Associated Fibroblasts in undifferentiated Nasopharyngeal Carcinoma: A putative role for the EBV-Encoded Oncoprotein, LMP1. Pathogens, 9 (1): 8
Murata, T. (2023) Epstein-Barr virus: The molecular virology and the associated diseases. Fujita Med J, 9 (2): 65-72
Narang, R., Manchanda, A., Kaur, H. (2019) Evaluation of a case of diffuse large B-cell lymphoma. J Oral Maxillofac Pathol, 2019 23 (Suppl 1): S7-11
Navarro, J.T., Moltó, J., Tapia, G., Ribera, J.M. (2021) Hodgkin Lymphoma in people living with HIV. Cancers (Basel), 13 (17): 4366
1
Odumade, O.A., Hogquist, K.A., Balfour, H.H. (2011) Progress and problems in understanding and managing primary Epstein-Barr virus infections. Clin Microbiol Rev, 24(1): 193-209
Oeckinghaus, A., Ghosh, S. (2009) The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb Perspect Biol, 1 (4): a000034
Ouaguia, L., Mrizak, D., Renaud, S., Moralès, O., Delhem, N. (2014) Control of the Inflammatory Response Mechanisms Mediated by Natural and Induced Regulatory T-Cells in HCV-, HTLV-1-, and EBV-Associated Cancers. Mediators Inflamm, 564296-564296
Pagano, J.S. (2007) Is Epstein-Barr virus transmitted sexually?. J Infect Dis, 195 (4): 469-470
Patini, R., Cordaro, M., Marchesini, D., Scilla, F., Gioco, G., Rupe, C., et al. (2023) Is Systemic Immunosuppression a Risk Factor for Oral Cancer? A Systematic Review and Meta-Analysis. Cancers (Basel), 15: 3077-3077
Pennacchiotti, G., Álvarez, C., Montes, R., Cárcamo, M., Sáez, R., Martínez, M.J. (2020) International journal of oral and dental health Epstein-Barr virus in oral cavity squamous cell carcinoma of Chilean patients. Int J Oral Dent Health, 6: 106-106
Petrara, M.R., Giunco, S., Serraino, D., Dolcetti, R., de Rossi, A. (2015) Post-transplant lymphoproliferative disorders: From epidemiology to pathogenesis-driven treatment. Cancer Letters, 369(1): 37-44
Pua, L.J.W., Mai, C.W., Chung, F.F.L., Khoo, A.S.B., Leong, C.O., Lim, W.M., et al. (2024) Functional roles of JNK and p38 MAPK signaling in nasopharyngeal carcinoma. Int J Mol Sci, 23 (3): 1108
Quinlan, S.C., Landgren, O., Morton, L.M., Engels, E.A. (2010) Hodgkin Lymphoma among U.S. Solid organ transplant recipients. Transplantation, 90 (9): 1011-5
Ren, X., Cheng, Y., Wu, S., Zeng, X., Shi, X., Ling, Q., et al. (2020) Primary non-Hodgkin lymphoma of the tongue base: The clinicopathology of seven cases and evaluation of HPV and EBV status. Diagn Pathol, 15 (1): 30
Richardo, T., Prattapong, P., Ngernsombat, C., Wisetyaningsih, N., Iizasa, H., Yoshiyama, H., et al. (2020) Epstein-Barr virus mediated signaling in nasopharyngeal carcinoma carcinogenesis. Cancers (Basel), 12(9): 2441-2441
Rivera-Soto, R., Damania, B. (2019) Modulation of Angiogenic processes by the human Gammaherpesviruses, Epstein-Barr virus and Kaposi’s sarcoma-associated Herpesvirus. Frontiers in Microbiology, 10: 1544-1544
Rochford, R. (2021) Reframing Burkitt lymphoma: Virology not epidemiology defines clinical variants. Ann Lymphoma, 5 : 22
Roschewski, M., Staudt, L.M., Wilson, W.H. (2022) Burkitt’s Lymphoma. N Engl J Med, 387 (12): 1111-1122
Rosemarie, Q., Sugden, B. (2020) Epstein-Barr virus: How its Lytic phase contributes to Oncogenesis. Microorganisms, 8(11): 1824-1824
Rostgaard, K., Balfour, H.H., Jarrett, R., Erikstrup, C., Pedersen, O., Ullum, H., et al. (2019) Primary Epstein-Barr virus infection with and without infectious mononucleosis. PLoS One, 14 (12): e0226436
Rühl, J., Leung, C.S., Münz, C. (2020) Vaccination against the Epstein-Barr virus. Cell Mol Life Sci, 77(21): 4315-4324
Sako, K., Kenzaka, T., Kumabe, A. (2023) Epstein-Barr virus-associated infectious mononucleosis with acute epididymitis: A case report. BMC Infect Dis, 22 (1): 147
1
Sausen, D.G., Bhutta, M.S., Gallo, E.S., Dahari, H., Borenstein, R. (2021) Stress-induced Epstein-Barr virus reactivation. Biomolecules, 11(9): 1380-1380
Shah, K.M., Young, L.S. (2009) Epstein-Barr virus and carcinogenesis: Beyond Burkitt’s lymphoma. Clin Microbiol Infect, 15(11): 982-988
Shanbhag, S., Ambinder, R.F. (2018) Hodgkin lymphoma: A review and update on recent progress. CA Cancer J Clin, 68(2): 116-132
Shannon-Lowe, C., Rickinson, A.B., Bell, A.I. (2017) Epstein-Barr virus-associated lymphomas. Philos Trans R Soc Lond B Biol Sci, 372 (1732): 20160271
Sharifipour, S., Rad, D.K. (2020) Seroprevalence of Epstein-Barr virus among children and adults in Tehran, Iran. New Microbes New Infect, 34 : 100641
1
Sharma, Y., Mishra, G., Parikh, V. (2019) Quality of life in head and neck cancer patients. Indian J Otolaryngol Head Neck Surg, 71 (1): 927-932
Shindiapina, P., Ahmed, E.H., Mozhenkova, A., Abebe, T., Baiocchi, R.A. (2020) Immunology of EBV-Related Lymphoproliferative Disease in HIV-Positive Individuals. Front Oncol, 10: 1723-1723
Singh, N., Baby, D., Rajguru, J., Patil, P., Thakkannavar, S., Pujari, V. (2019) Inflammation and cancer. Ann Afr Med, 18 (3):121-126
Spence, T., Bruce, J., Yip, K.W., Liu, F.F. (2016) MicroRNAs in nasopharyngeal carcinoma. Chin Clin Oncol, 5 (2): 17
Spina, M., Carbone, A., Gloghini, A., Serraino, D., Berretta, M., Tirelli, U. (2011) Hodgkin’s Disease in Patients with HIV Infection. Adv Hematol, 402682
Stowe, R.P., Kozlova, E.V., Yetman, D.L., Walling, D.M., Goodwin, J.S., Glaser, R. (2007) Chronic herpesvirus reactivation occurs in aging. Exp Gerontol, 42 (6): 563-570
Styles, C.T., Paschos, K., White, R.E., Farrell, P.J. (2018) The cooperative functions of the EBNA3 proteins are central to EBV persistence and latency. Pathogens, 7(1): 31-31
Szymula, A., Palermo, R.D., Bayoumy, A., Groves, I.J., Ba, A.M., Holder, B., White, R.E. (2018) Correction: Epstein-Barr virus nuclear antigen EBNA-LP is essential for transforming naïve B cells, and facilitates recruitment of transcription factors to the viral genome. PLoS Pathogens, 15(2): e1007403-e1007403
Thandra, K.C., Barsouk, A., Saginala, K., Padala, S.A., Barsouk, A., Rawla, P. (2021) Epidemiology of Non-hodgkin’s Lymphoma. Medical Sciences, 9(1): 5-5
Tsang, C.M., Deng, W., Yip, Y.L., Zeng, M.S., Lo, K.W., Tsao, S.W. (2014) Epstein-Barr virus infection and persistence in nasopharyngeal epithelial cells. Chin J Cancer, 33 (11): 549-55
Tsao, S.W., Tsang, C.M., Lo, K.W. (2017) Epstein-Barr virus infection and nasopharyngeal carcinoma. Philos Trans R Soc Lond B Biol Sci, 372 (1732): 20160270
Tsao, S.W., Tsang, C.M., To, K.F., Lo, K.W. (2015) The role of Epstein-Barr virus in epithelial malignancies. J Pathol, 235(2): 323-333
Tse, E., Kwong, Y.L. (2017) The diagnosis and management of NK/T-cell lymphomas. Journal of Hematology & Oncology, 10 (1): 85
van Zuylen, W.J., Rawlinson, W.D., Ford, C.E. (2016) The Wnt pathway: A key network in cell signalling dysregulated by viruses. Rev Med Virol, 26 (5) :b340-355
Velapasamy, S., Dawson, C.W., Young, L.S., Paterson, I.C., Yap, L.F. (2018) The dynamic roles of TGF-b Signalling in EBV-Associated Cancers. Cancers (Basel), 10 (8): 247
Vockerodt, M., Cader, F.Z., Shannon-Lowe, C., Murray, P. (2014) Epstein-Barr virus and the origin of Hodgkin lymphoma. Chin J Cancer, 33(12): 591-597
Wakae, K., Kondo, S., Pham, H.T., Wakisaka, N., Que, L., Li, Y., Zheng, X., Fukano, K., Kitamura, K., Watashi, K., Aizaki, H., Ueno, T., Moriyama-Kita, M., Ishikawa, K., Nakanishi, Y., Endo, K. (2020) EBV-LMP1 induces APOBEC3s and mitochondrial DNA hypermutation in nasopharyngeal cancer. Cancer Medicine, 9(20): 7663-7671
Yan, M., Xu, Q., Zhang, P., Zhou, X.J., Zhang, Z.Y., Chen, W.T. (2010) Correlation of NF-cB signal pathway with tumor metastasis of human head and neck squamous cell carcinoma. BMC Cancer, 10: 437-437
Young, L.S., Dawson, C.W. (2014) Epstein-Barr virus and nasopharyngeal carcinoma. Chin J Cancer, 33 (12): 581-590
Zhang, W., Guo, Q., Liu, G., Zheng, F., Chen, J., Huang, D., et al. (2019) NKILA represses nasopharyngeal carcinoma carcinogenesis and metastasis by NF-cB pathway inhibition. PLoS Genet, 15 (8): e1008325
Zhao, H., Wu, L., Yan, G., Chen, Y., Zhou, M., Wu, Y., et al. (2021) Inflammation and tumor progression: Signaling pathways and targeted intervention. Signal Transduct Target Ther, 6(1): 263-263
Zhou, X., Cui, J., Macias, V., Ye, H., Wang, J., Rao, P.N. (2007) The progress on genetic analysis of nasopharyngeal carcinoma. Comp Funct Genomics, 57513
Zhu, Q.Y., Zhao, G.X., Li, Y., Talakatta, G., Mai, H.Q., Le, Q.T., et al. (2021) Advances in pathogenesis and precision medicine for nasopharyngeal carcinoma. Med Comm, 2(2): 175-206
Balkan Journal of Dental Medicine, 2024, vol. 28, br. 1, str. 1-15