Research ArticleOriginal Article

Epstein-Barr virus DNA loads in the peripheral blood cells predict the survival of locoregionally-advanced nasopharyngeal carcinoma patients

Yongqiao He, Dawei Yang, Ting Zhou, Wenqiong Xue, Jiangbo Zhang, Fangfang Li, Fang Wang, Tongmin Wang, Ziyi Wu, Ying Liao, Meiqi Zheng, Changmi Deng, Danhua Li, Yijing Jia, Leilei Yuan, Wenli Zhang and Weihua Jia
Cancer Biology & Medicine August 2021, 18 (3) 888-899; DOI: https://doi.org/10.20892/j.issn.2095-3941.2020.0464

References

  1. 1.↵
    2. Plummer M,
    3. de Martel C,
    4. Vignat J,
    5. Ferlay J,
    6. Bray F,
    7. Franceschi S.
    Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health. 2016; 4: e609–16.
    OpenUrl
  2. 2.↵
    2. Klein G.
    Nasopharyngeal carcinoma (NPC) is an enigmatic tumor. Semin Cancer Biol. 2002; 12: 415–8.
    OpenUrlCrossRefPubMed
  3. 3.↵
    2. Wei KR,
    3. Zheng RS,
    4. Zhang SW,
    5. Liang ZH,
    6. Li ZM,
    7. Chen WQ.
    Nasopharyngeal carcinoma incidence and mortality in China, 2013. Chin J Cancer. 2017; 36: 90.
    OpenUrlCrossRefPubMed
  4. 4.
    2. Tao Q,
    3. Chan AT.
    Nasopharyngeal carcinoma: molecular pathogenesis and therapeutic developments. Expert Rev Mol Med. 2007; 9: 1–24.
    OpenUrlCrossRefPubMed
  5. 5.
    2. Lee AW,
    3. Fee Jr WE,
    4. Ng WT,
    5. Chan LK.
    Nasopharyngeal carcinoma: salvage of local recurrence. Oral Oncol. 2012; 48: 768–74.
    OpenUrlCrossRefPubMed
  6. 6.↵
    2. Feng RM,
    3. Zong YN,
    4. Cao SM,
    5. Xu RH.
    Current cancer situation in China: good or bad news from the 2018 Global Cancer Statistics? Cancer Commun (Lond). 2019; 39: 22.
    OpenUrl
  7. 7.↵
    2. Mao YP,
    3. Xie FY,
    4. Liu LZ,
    5. Sun Y,
    6. Li L,
    7. Tang LL, et al.
    Re-evaluation of 6th edition of AJCC staging system for nasopharyngeal carcinoma and proposed improvement based on magnetic resonance imaging. Int J Radiat Oncol Biol Phys. 2009; 73: 1326–34.
    OpenUrlCrossRefPubMed
  8. 8.↵
    2. Chen YP,
    3. Chan ATC,
    4. Le QT,
    5. Blanchard P,
    6. Sun Y,
    7. Ma J.
    Nasopharyngeal carcinoma. Lancet. 2019; 394: 64–80.
    OpenUrlCrossRefPubMed
  9. 9.↵
    2. Babcock GJ,
    3. Decker LL,
    4. Volk M,
    5. Thorley-Lawson DA.
    EBV persistence in memory B cells in vivo. Immunity. 1998; 9: 395–404.
    OpenUrlCrossRefPubMedWeb of Science
  10. 10.
    2. Henle G,
    3. Henle W,
    4. Clifford P,
    5. Diehl V,
    6. Kafuko GW,
    7. Kirya BG, et al.
    Antibodies to Epstein-Barr virus in Burkitt’s lymphoma and control groups. J Natl Cancer Inst. 1969; 43: 1147–57.
    OpenUrlPubMedWeb of Science
  11. 11.↵
    2. Tsao SW,
    3. Tsang CM,
    4. Lo KW.
    Epstein-Barr virus infection and nasopharyngeal carcinoma. Philos Trans R Soc Lond B Biol Sci. 2017; 372: 20160270.
    OpenUrlCrossRefPubMed
  12. 12.↵
    2. Kim KY,
    3. Le QT,
    4. Yom SS,
    5. Ng RHW,
    6. Chan KCA,
    7. Bratman SV, et al.
    Clinical utility of Epstein-Barr virus DNA testing in the treatment of nasopharyngeal carcinoma patients. Int J Radiat Oncol Biol Phys. 2017; 98: 996–1001.
    OpenUrlCrossRef
  13. 13.↵
    2. Kanakry J,
    3. Ambinder R.
    The biology and clinical uof EBV monitoring in blood. Curr Top Microbiol Immunol. 2015; 391: 475–99.
    OpenUrl
  14. 14.↵
    2. Smatti MK,
    3. Al-Sadeq DW,
    4. Ali NH,
    5. Pintus G,
    6. Abou-Saleh H,
    7. Nasrallah GK.
    Epstein-Barr virus epidemiology, serology, and genetic variability of LMP-1 oncogene among healthy population: an update. Front Oncol. 2018; 8: 211.
    OpenUrlPubMed
  15. 15.↵
    2. Chan KCA,
    3. Woo JKS,
    4. King A,
    5. Zee BCY,
    6. Lam WKJ,
    7. Chan SL, et al.
    Analysis of plasma Epstein-Barr virus DNA to screen for nasopharyngeal cancer. N Engl J Med. 2017; 377: 513–22.
    OpenUrlCrossRefPubMed
  16. 16.↵
    2. Tang LQ,
    3. Li CF,
    4. Li J,
    5. Chen WH,
    6. Chen QY,
    7. Yuan LX, et al.
    Establishment and validation of prognostic nomograms for endemic nasopharyngeal carcinoma. J Natl Cancer Inst. 2016; 108: 291.
    OpenUrl
  17. 17.
    2. Huang CL,
    3. Sun ZQ,
    4. Guo R,
    5. Liu X,
    6. Mao YP,
    7. Peng H, et al.
    Plasma Epstein-Barr virus DNA load after induction chemotherapy predicts outcome in locoregionally advanced nasopharyngeal carcinoma. Int J Radiat Oncol Biol Phys. 2019; 104: 355–61.
    OpenUrl
  18. 18.↵
    2. Lv J,
    3. Chen Y,
    4. Zhou G,
    5. Qi Z,
    6. Tan KRL,
    7. Wang H, et al.
    Liquid biopsy tracking during sequential chemo-radiotherapy identifies distinct prognostic phenotypes in nasopharyngeal carcinoma. Nat Commun. 2019; 10: 3941.
    OpenUrl
  19. 19.
    2. Lam WKJ,
    3. Chan KCA,
    4. Lo YMD.
    Plasma Epstein-Barr virus DNA as an archetypal circulating tumour DNA marker. J Pathol. 2019; 247: 641–9.
    OpenUrl
  20. 20.↵
    2. Peng L,
    3. Yang Y,
    4. Guo R,
    5. Mao YP,
    6. Xu C,
    7. Chen YP, et al.
    Relationship between pretreatment concentration of plasma Epstein-Barr virus DNA and tumor burden in nasopharyngeal carcinoma: an updated interpretation. Cancer Med. 2018; 7: 5988–98.
    OpenUrl
  21. 21.
    2. Ma BB,
    3. King A,
    4. Lo YM,
    5. Yau YY,
    6. Zee B,
    7. Hui EP, et al.
    Relationship between pretreatment level of plasma Epstein-Barr virus DNA, tumor burden, and metabolic activity in advanced nasopharyngeal carcinoma. Int J Radiat Oncol Biol Phys. 2006; 66: 714–20.
    OpenUrlCrossRefPubMedWeb of Science
  22. 22.↵
    2. Lo YM,
    3. Chan AT,
    4. Chan LY,
    5. Leung SF,
    6. Lam CW,
    7. Huang DP, et al.
    Molecular prognostication of nasopharyngeal carcinoma by quantitative analysis of circulating Epstein-Barr virus DNA. Cancer Res. 2000; 60: 6878–81.
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    2. Thorley-Lawson DA,
    3. Miyashita EM,
    4. Khan G.
    Epstein-Barr virus and the B cell: that’s all it takes. Trends Microbiol. 1996; 4: 204–8.
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.↵
    2. Yao QY,
    3. Rickinson AB,
    4. Epstein MA.
    A re-examination of the Epstein-Barr virus carrier state in healthy seropositive individuals. Int J Cancer. 1985; 35: 35–42.
    OpenUrlCrossRefPubMedWeb of Science
  25. 25.↵
    2. Shao JY,
    3. Zhang Y,
    4. Li YH,
    5. Gao HY,
    6. Feng HX,
    7. Wu QL, et al.
    Comparison of Epstein-Barr virus DNA level in plasma, peripheral blood cell and tumor tissue in nasopharyngeal carcinoma. Anticancer Res. 2004; 24: 4059–66.
    OpenUrlAbstract/FREE Full Text
  26. 26.↵
    2. Kanakry JA,
    3. Hegde AM,
    4. Durand CM,
    5. Massie AB,
    6. Greer AE,
    7. Ambinder RF, et al.
    The clinical significance of EBV DNA in the plasma and peripheral blood mononuclear cells of patients with or without EBV diseases. Blood. 2016; 127: 2007–17.
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    2. Wang WY,
    3. Chien YC,
    4. Jan JS,
    5. Chueh CM,
    6. Lin JC.
    Consistent sequence variation of Epstein-Barr virus nuclear antigen 1 in primary tumor and peripheral blood cells of patients with nasopharyngeal carcinoma. Clin Cancer Res. 2002; 8: 2586–90.
    OpenUrlAbstract/FREE Full Text
  28. 28.↵
    2. He YQ,
    3. Liao XY,
    4. Xue WQ,
    5. Xu YF,
    6. Xu FH,
    7. Li FF, et al.
    Association between environmental factors and oral Epstein-Barr virus DNA loads: a multicenter cross-sectional study in China. J Infect Dis. 2019; 219: 400–9.
    OpenUrl
  29. 29.↵
    2. Lo YM,
    3. Chan LY,
    4. Lo KW,
    5. Leung SF,
    6. Zhang J,
    7. Chan AT, et al.
    Quantitative analysis of cell-free Epstein-Barr virus DNA in plasma of patients with nasopharyngeal carcinoma. Cancer Res. 1999; 59: 1188–91.
    OpenUrlAbstract/FREE Full Text
  30. 30.↵
    2. Lay ML,
    3. Lucas RM,
    4. Ratnamohan M,
    5. Taylor J,
    6. Ponsonby AL,
    7. Dwyer DE, et al.
    Measurement of Epstein-Barr virus DNA load using a novel quantification standard containing two EBV DNA targets and SYBR Green I dye. Virol J. 2010; 7: 252.
    OpenUrlPubMed
  31. 31.↵
    2. Zhou GQ,
    3. Tang LL,
    4. Mao YP,
    5. Chen L,
    6. Li WF,
    7. Sun Y, et al.
    Baseline serum lactate dehydrogenase levels for patients treated with intensity-modulated radiotherapy for nasopharyngeal carcinoma: a predictor of poor prognosis and subsequent liver metastasis. Int J Radiat Oncol Biol Phys. 2012; 82: e359–65.
    OpenUrlCrossRefPubMed
  32. 32.↵
    2. Chua ML,
    3. Tan SH,
    4. Kusumawidjaja G,
    5. Shwe MT,
    6. Cheah SL,
    7. Fong KW, et al.
    Neutrophil-to-lymphocyte ratio as a prognostic marker in locally advanced nasopharyngeal carcinoma: a pooled analysis of two randomised controlled trials. Eur J Cancer. 2016; 67: 119–29.
    OpenUrl
  33. 33.↵
    2. Kedi W,
    3. Dongjiang X,
    4. Zhi L,
    5. Yan G,
    6. Kun J,
    7. Jianrong S.
    The rational specimen for the quantitative detection of Epstein-Barr virus DNA load. Clin Chem Lab Med. 2019; 57: 759–65.
    OpenUrl
  34. 34.
    2. Chen HS,
    3. Ho MC,
    4. Hu RH,
    5. Wu JF,
    6. Chen HL,
    7. Ni YH, et al.
    Roles of Epstein-Barr virus viral load monitoring in the prediction of posttransplant lymphoproliferative disorder in pediatric liver transplantation. J Formos Med Assoc. 2019; 118: 1362–8.
    OpenUrl
  35. 35.↵
    2. Leruez-Ville M,
    3. Seng R,
    4. Morand P,
    5. Boufassa F,
    6. Boue F,
    7. Deveau C, et al.
    Blood Epstein-Barr virus DNA load and risk of progression to AIDS-related systemic B lymphoma. HIV Med. 2012; 13: 479–87.
    OpenUrlPubMedWeb of Science
  36. 36.↵
    2. Lin JC,
    3. Chen KY,
    4. Wang WY,
    5. Jan JS,
    6. Liang WM,
    7. Tsai CS, et al.
    Detection of Epstein-Barr virus DNA in the peripheral-blood cells of patients with nasopharyngeal carcinoma: relationship to distant metastasis and survival. J Clin Oncol. 2001; 19: 2607–15.
    OpenUrlAbstract/FREE Full Text
  37. 37.↵
    2. Shen Y,
    3. Zhang S,
    4. Sun R,
    5. Wu T,
    6. Qian J.
    Understanding the interplay between host immunity and Epstein-Barr virus in NPC patients. Emerg Microbes Infect. 2015; 4: e20.
  38. 38.↵
    2. Liu SL,
    3. Sun XS,
    4. Li XY,
    5. Tang LQ,
    6. Chen QY,
    7. Lin HX, et al.
    The diagnostic and prognostic values of plasma Epstein-Barr virus DNA for residual cervical lymphadenopathy in nasopharyngeal carcinoma patients: a retrospective study. Cancer Commun (Lond). 2019; 39: 14.
    OpenUrl
  39. 39.↵
    2. Lin JC,
    3. Wang WY,
    4. Chen KY,
    5. Wei YH,
    6. Liang WM,
    7. Jan JS, et al.
    Quantification of plasma Epstein-Barr virus DNA in patients with advanced nasopharyngeal carcinoma. N Engl J Med. 2004; 350: 2461–70.
    OpenUrlCrossRefPubMedWeb of Science
  40. 40.↵
    2. Kanakry JA,
    3. Li H,
    4. Gellert LL,
    5. Lemas MV,
    6. Hsieh WS,
    7. Hong F, et al.
    Plasma Epstein-Barr virus DNA predicts outcome in advanced Hodgkin lymphoma: correlative analysis from a large North American cooperative group trial. Blood. 2013; 121: 3547–53.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    2. Gandhi MK,
    3. Lambley E,
    4. Burrows J,
    5. Dua U,
    6. Elliott S,
    7. Shaw PJ, et al.
    Plasma Epstein-Barr virus (EBV) DNA is a biomarker for EBV-positive Hodgkin’s lymphoma. Clin Cancer Res. 2006; 12: 460–4.
    OpenUrlAbstract/FREE Full Text
  42. 42.↵
    2. Wagner HJ,
    3. Wessel M,
    4. Jabs W,
    5. Smets F,
    6. Fischer L,
    7. Offner G, et al.
    Patients at risk for development of posttransplant lymphoproliferative disorder: plasma versus peripheral blood mononuclear cells as material for quantification of Epstein-Barr viral load by using real-time quantitative polymerase chain reaction. Transplantation. 2001; 72: 1012–9.
    OpenUrlCrossRefPubMedWeb of Science
  43. 43.↵
    2. Hakim H,
    3. Gibson C,
    4. Pan J,
    5. Srivastava K,
    6. Gu Z,
    7. Bankowski MJ, et al.
    Comparison of various blood compartments and reporting units for the detection and quantification of Epstein-Barr virus in peripheral blood. J Clin Microbiol. 2007; 45: 2151–5.
    OpenUrlAbstract/FREE Full Text
  44. 44.↵
    2. Gotoh K,
    3. Ito Y,
    4. Ohta R,
    5. Iwata S,
    6. Nishiyama Y,
    7. Nakamura T, et al.
    Immunologic and virologic analyses in pediatric liver transplant recipients with chronic high Epstein-Barr virus loads. J Infect Dis. 2010; 202: 461–9.
    OpenUrlPubMed
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