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Research Paper

Presence of high-risk HPVs, EBV, and MMTV in human triple-negative breast cancer

ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 4457-4466 | Received 23 Jun 2021, Accepted 26 Aug 2021, Published online: 08 Oct 2021

References

  • Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Piñeros M, Znaor A, Bray F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144(8):1941–53. doi:10.1002/ijc.31937.
  • Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747–52. doi:10.1038/35021093.
  • Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A. 2003;100(14):8418–23. doi:10.1073/pnas.0932692100.
  • Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med. 2010;363(20):1938–48. doi:10.1056/NEJMra1001389.
  • Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987;235(4785):177–82. doi:10.1126/science.3798106.
  • Putti TC, El-Rehim DM, Rakha EA, Paish CE, Lee AH, Pinder SE, Ellis IO. Estrogen receptor-negative breast carcinomas: a review of morphology and immunophenotypical analysis. Mod Pathol. 2005;18(1):26–35. doi:10.1038/modpathol.3800255.
  • Irvin WJ Jr., Carey LA. What is triple-negative breast cancer? Eur J Cancer. 2008;44(18):2799–805. doi:10.1016/j.ejca.2008.09.034.
  • Stockmans G, Deraedt K, Wildiers H, Moerman P, Paridaens R. Triple-negative breast cancer. Curr Opin Oncol. 2008;20(6):614–20. doi:10.1097/CCO.0b013e328312efba.
  • Venuti A, Badaracco G, Rizzo C, Mafera B, Rahimi S, Vigili M. Presence of HPV in head and neck tumours: high prevalence in tonsillar localization. J Exp Clin Cancer Res. 2004;23:561–66.
  • Ragin CC, Taioli E. Survival of squamous cell carcinoma of the head and neck in relation to human papillomavirus infection: review and meta-analysis. Int J Cancer. 2007;121(8):1813–20. doi:10.1002/ijc.22851.
  • Shi Y, Peng SL, Yang LF, Chen X, Tao YG, Cao Y. Co-infection of Epstein-Barr virus and human papillomavirus in human tumorigenesis. Chin J Cancer. 2016;35(1):16. doi:10.1186/s40880-016-0079-1.
  • Deligdisch L, Marin T, Lee AT, Etkind P, Holland JF, Melana S, Pogo BGT, Deligdisch L, Marin T, Lee AT, et al. Human mammary tumor virus (HMTV) in endometrial carcinoma. Int J Gynecol Cancer. 2013;23(8):1423–28. doi:10.1097/IGC.0b013e3182980fc5.
  • Johal H, Faedo M, Faltas J, Lau A, Mousina R, Cozzi P, deFazio A, Rawlinson WD. DNA of mouse mammary tumor virus-like virus is present in human tumors influenced by hormones. J Med Virol. 2010;82(6):1044–50. doi:10.1002/jmv.21754.
  • Tulay P, Serakinci N. The route to HPV-associated neoplastic transformation: a review of the literature. Crit Rev Eukaryot Gene Expr. 2016;26(1):27–39. doi:10.1615/CritRevEukaryotGeneExpr.v26.i1.40.
  • Ferreira AR, Ramalho AC, Marques M, Ribeiro D. The interplay between antiviral signalling and carcinogenesis in human papillomavirus infections. Cancers (Basel). 2020;12(3):646.
  • Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer. 2010;10(8):550–60. doi:10.1038/nrc2886.
  • Al Moustafa AE. E5 and E6/E7 of high-risk HPVs cooperate to enhance cancer progression through EMT initiation. Cell Adh Migr. 2015;9(5):392–93. doi:10.1080/19336918.2015.1042197.
  • Chen X, Bode AM, Dong Z, Cao Y. The epithelial-mesenchymal transition (EMT) is regulated by oncoviruses in cancer. Faseb J. 2016;30(9):3001–10. doi:10.1096/fj.201600388R.
  • Al-Thawadi H, Gupta I, Jabeen A, Skenderi F, Aboulkassim T, Yasmeen A, Malki MI, Batist G, Vranic S, Al Moustafa A-E, et al. Co-presence of human papillomaviruses and Epstein–Barr virus is linked with advanced tumor stage: a tissue microarray study in head and neck cancer patients. Cancer Cell Int. 2020;20(1):361. doi:10.1186/s12935-020-01348-y.
  • Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. Human papillomavirus and cervical cancer. Lancet. 2007;370(9590):890–907. doi:10.1016/S0140-6736(07)61416-0.
  • Li N, Yang L, Zhang Y, Zhao P, Zheng T, Dai M. Human papillomavirus infection and bladder cancer risk: a meta-analysis. J Infect Dis. 2011;204(2):217–23. doi:10.1093/infdis/jir248.
  • Akil N, Yasmeen A, Kassab A, Ghabreau L, Darnel AD, Al Moustafa A-E. High-risk human papillomavirus infections in breast cancer in Syrian women and their association with Id-1 expression: a tissue microarray study. Br J Cancer. 2008;99(3):404–07. doi:10.1038/sj.bjc.6604503.
  • Bedri S, Sultan AA, Alkhalaf M, Al Moustafa A-E, Vranic S. Epstein-Barr virus (EBV) status in colorectal cancer: a mini review. Hum Vaccin Immunother. 2019;15(3):603–10. doi:10.1080/21645515.2018.1543525.
  • Young LS, Arrand JR, Murray PG. EBV gene expression and regulation. In: Arvin AC-FG, Mocarski E, et al., editors. Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge: Cambridge University Press; 2007.
  • Cyprian FS, Al-Farsi HF, Vranic S, Akhtar S, Al Moustafa AE. Epstein-Barr virus and human papillomaviruses interactions and their roles in the initiation of epithelial-mesenchymal transition and cancer progression. Front Oncol. 2018;8:111. doi:10.3389/fonc.2018.00111.
  • 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. doi:10.1053/hupa.2002.129786.
  • Boudreault S, Armero VES, Scott MS, Perreault J-P, Bisaillon M. The Epstein-Barr virus EBNA1 protein modulates the alternative splicing of cellular genes. Virol J. 2019;16(1):29. doi:10.1186/s12985-019-1137-5.
  • Bittner JJ. Some possible effects of nursing on the mammary gland tumor incidence in mice. Science. 1936;84(2172):162. doi:10.1126/science.84.2172.162.
  • Mason A. Is there a breast cancer virus? Ochsner J. 2000;2:36–39.
  • Lawson JS, Günzburg WH, Whitaker NJ. Viruses and human breast cancer. Future Microbiol. 2006;1(1):33–51. doi:10.2217/17460913.1.1.33.
  • Nartey T, Moran H, Marin T, Arcaro KF, Anderton DL, Etkind P, Holland JF, Melana SM, Pogo BGT. Human mammary tumor virus (HMTV) sequences in human milk. Infect Agent Cancer. 2014;9(1):20. doi:10.1186/1750-9378-9-20.
  • Mazzanti CM, Lessi F, Armogida I, Zavaglia K, Franceschi S, Al Hamad M, Roncella M, Ghilli M, Boldrini A, Aretini P, et al. Human saliva as route of inter-human infection for mouse mammary tumor virus. Oncotarget. 2015;6(21):18355–63. doi:10.18632/oncotarget.4567.
  • Lushnikova AA, Kriukova IN, Malivanova TF, Makhov PB, Polevaia EB. Correlation between expression of antigen immunologically related to gp52 MMTV and transcription of homologous ENV MMTV DNA sequences in peripheral blood lymphocytes from breast cancer patients. Mol Gen Mikrobiol Virusol. 1998:33–36.
  • Dudley JP, Golovkina TV, Ross SR. Lessons learned from mouse mammary tumor virus in animal models. ILAR J. 2016;57(1):12–23. doi:10.1093/ilar/ilv044.
  • Al Moustafa A-E, Al-Awadhi R, Missaoui N, Adam I, Durusoy R, Ghabreau L, Akil N, Ahmed HG, Yasmeen A, Alsbeih G, et al. Human papillomaviruses-related cancers. Presence and prevention strategies in the Middle east and north African regions. Hum Vaccin Immunother. 2014;10(7):1812–21. doi:10.4161/hv.28742.
  • Gupta I, Jabeen A, Al-Sarraf R, Farghaly H, Vranic S, Sultan AA, Al Moustafa A-E, Al-Thawadi H. The co-presence of high-risk human papillomaviruses and Epstein-Barr virus is linked with tumor grade and stage in Qatari women with breast cancer. Hum Vaccin Immunother. 2021;17(4):982–89. doi:10.1080/21645515.2020.1802977.
  • Al Hamad M, Matalka I, Al Zoubi MS, Armogida I, Khasawneh R, Al-Husaini M, et al. Human mammary tumor virus, human papilloma virus, and Epstein-Barr virus infection are associated with sporadic breast cancer metastasis. Breast Cancer: Basic Clin Res. 2020;14:1178223420976388.
  • Lawson JS, Heng B. Viruses and breast cancer. Cancers. 2010;2(2):752–72. doi:10.3390/cancers2020752.
  • De Cremoux P, Thioux M, Lebigot I, Sigal-Zafrani B, Salmon R, Sastre-Garau X. No evidence of human papillomavirus DNA sequences in invasive breast carcinoma. Breast Cancer Res Treat. 2008;109(1):55–58. doi:10.1007/s10549-007-9626-4.
  • Herrmann K, Niedobitek G. Lack of evidence for an association of Epstein–Barr virus infection with breast carcinoma. Breast Cancer Res. 2002;5(1):R13. doi:10.1186/bcr561.
  • Amarante MK, de Sousa Pereira N, Vitiello GAF, Watanabe MAE. Involvement of a mouse mammary tumor virus (MMTV) homologue in human breast cancer: evidence for, against and possible causes of controversies. Microb Pathog. 2019;130:283–94. doi:10.1016/j.micpath.2019.03.021.
  • Al Moustafa A-E, Al-Antary N, Aboulkassim T, Akil N, Batist G, Yasmeen A. Co-prevalence of Epstein-Barr virus and high-risk human papillomaviruses in Syrian women with breast cancer. Hum Vaccin Immunother. 2016;12:1936–39.
  • Al-Thawadi H, Ghabreau L, Aboulkassim T, Yasmeen A, Vranic S, Batist G, Al Moustafa A-E. Co-incidence of Epstein–Barr virus and high-risk human papillomaviruses in cervical cancer of Syrian women. Front Oncol. 2018;8:250. doi:10.3389/fonc.2018.00250.
  • Malki MI, Gupta I, Fernandes Q, Aboulkassim T, Yasmeen A, Vranic S, Al Moustafa A-E, Al-Thawadi HA. Co-presence of Epstein–Barr virus and high-risk human papillomaviruses in Syrian colorectal cancer samples. Hum Vaccin Immunother. 2020;16(10):2403–07. doi:10.1080/21645515.2020.1726680.
  • Lawson JS, Glenn WK. Evidence for a causal role by mouse mammary tumour-like virus in human breast cancer. NPJ Breast Cancer. 2019;5(1):40. doi:10.1038/s41523-019-0136-4.
  • Allison KH, Hammond MEH, Dowsett M, McKernin SE, Carey LA, Fitzgibbons PL, Hayes DF, Lakhani SR, Chavez-MacGregor M, Perlmutter J, et al. Estrogen and progesterone receptor testing in breast cancer: ASCO/CAP guideline update. J Clin Oncol. 2020;38(12):1346–66. doi:10.1200/JCO.19.02309.
  • Wolff AC, Hammond MEH, Allison KH, Harvey BE, Mangu PB, Bartlett JMS, Bilous M, Ellis IO, Fitzgibbons P, Hanna W, et al. Human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline focused update. Arch Pathol Lab Med. 2018;142(11):1364–82. doi:10.5858/arpa.2018-0902-SA.
  • Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991;19(5):403–10. doi:10.1111/j.1365-2559.1991.tb00229.x.
  • Nagi K, Gupta I, Jurdi N, Jabeen A, Yasmeen A, Batist G, Vranic S, Al-Moustafa A-E. High-risk human papillomaviruses and Epstein–Barr virus in breast cancer in Lebanese women and their association with tumor grade: a molecular and tissue microarray study. Cancer Cell Int. 2021;21(1):308. doi:10.1186/s12935-021-02009-4.
  • Gupta I, Nasrallah GK, Sharma A, Jabeen A, Smatti MK, Al-Thawadi HA, Sultan AA, Alkhalaf M, Vranic S, Moustafa AEA, et al. Co-prevalence of human Papillomaviruses (HPV) and Epstein–Barr virus (EBV) in healthy blood donors from diverse nationalities in Qatar. Cancer Cell Int. 2020;20(1):107. doi:10.1186/s12935-020-01190-2.
  • Gupta I, Al Farsi H, Jabeen A, Skenderi F, Al-Thawadi H, AlAhmad YM, Abdelhafez I, Al Moustafa A-E, Vranic S. High-risk human papillomaviruses and Epstein–Barr virus in colorectal cancer and their association with clinicopathological status. Pathogens. 2020;9(6):452. doi:10.3390/pathogens9060452.
  • Xiao C-Y, Fu -B-B, Li Z-Y, Mushtaq G, Kamal MA, Li J-H, Tang G-C, Xiao -S-S. Observations on the expression of human papillomavirus major capsid protein in HeLa cells. Cancer Cell Int. 2015;15(1):53. doi:10.1186/s12935-015-0206-0.
  • Al Moustafa A-E, Foulkes WD, Benlimame N, Wong A, Yen L, Bergeron J, Batist G, Alpert L, Alaoui-Jamali MA. E6/E7 proteins of HPV type 16 and ErbB-2 cooperate to induce neoplastic transformation of primary normal oral epithelial cells. Oncogene. 2004;23(2):350–58. doi:10.1038/sj.onc.1207148.
  • May FE, Westley BR. Characterization of sequences related to the mouse mammary tumor virus that are specific to MCF-7 breast cancer cells. Cancer Res. 1989;49:3879–83.
  • Heng B, Glenn WK, Ye Y, Tran B, Delprado W, Lutze-Mann L, Whitaker NJ, Lawson JS. Human papilloma virus is associated with breast cancer. Br J Cancer. 2009;101(8):1345–50. doi:10.1038/sj.bjc.6605282.
  • Khodabandehlou N, Mostafaei S, Etemadi A, Ghasemi A, Payandeh M, Hadifar S, Norooznezhad AH, Kazemnejad A, Moghoofei M. Human papilloma virus and breast cancer: the role of inflammation and viral expressed proteins. BMC Cancer. 2019;19(1):61. doi:10.1186/s12885-019-5286-0.
  • Herrera-Goepfert R, Vela-Chávez T, Carrillo-García A, Lizano-Soberón M, Amador-Molina A, Oñate-Ocaña LF, Hallmann RSR. High-risk human papillomavirus (HPV) DNA sequences in metaplastic breast carcinomas of Mexican women. BMC Cancer. 2013;13(1):445. doi:10.1186/1471-2407-13-445.
  • Khan NA, Castillo A, Koriyama C, Kijima Y, Umekita Y, Ohi Y, Higashi M, Sagara Y, Yoshinaka H, Tsuji T, et al. Human papillomavirus detected in female breast carcinomas in Japan. Br J Cancer. 2008;99(3):408–14. doi:10.1038/sj.bjc.6604502.
  • Fernandes A, Bianchi G, Feltri AP, Pérez M, Correnti M. Presence of human papillomavirus in breast cancer and its association with prognostic factors. Ecancermedicalscience. 2015;9:548. doi:10.3332/ecancer.2015.548.
  • Sabol I, Milutin Gašperov N, Matovina M, Božinović K, Grubišić G, Fistonić I, Belci D, Alemany L, Džebro S, Dominis M, et al. Cervical HPV type-specific pre-vaccination prevalence and age distribution in Croatia. PLOS ONE. 2017;12(7):e0180480. doi:10.1371/journal.pone.0180480.
  • Grce M, Husnjak K, Magdić L, Ilijas M, Zlacki M, Lepusić D, Lukač J, Hodek B, Grizelj V, Kurjak A, et al. Detection and typing of human papillomaviruses by polymerase chain reaction in cervical scrapes of Croatian women with abnormal cytology. Eur J Epidemiol. 1997;13(6):645–51. doi:10.1023/A:1007323405069.
  • Grce M, Husnjak K, Bozikov J, Magdić L, Zlacki M, Lukac J, et al. Evaluation of genital human papillomavirus infections by polymerase chain reaction among Croatian women. Anticancer Res. 2001;21:579–84.
  • Delgado-García S, Martínez-Escoriza J-C, Alba A, Martín-Bayón T-A, Ballester-Galiana H, Peiró G, Caballero P, Ponce-Lorenzo J. Presence of human papillomavirus DNA in breast cancer: a Spanish case-control study. BMC Cancer. 2017;17(1):320. doi:10.1186/s12885-017-3308-3.
  • Frega A, Lorenzon L, Bononi M, De Cesare A, Ciardi A, Lombardi D, et al. Evaluation of E6 and E7 mRNA expression in HPV DNA positive breast cancer. Eur J Gynaecol Oncol. 2012;33:164–67.
  • Salman NA, Davies G, Majidy F, Shakir F, Akinrinade H, Perumal D, Ashrafi GH. Association of high risk human papillomavirus and breast cancer: a UK based study. Sci Rep. 2017;7(1):43591. doi:10.1038/srep43591.
  • de Villiers E-M, Sandstrom RE, zur Hausen H, Buck CE. Presence of papillomavirus sequences in condylomatous lesions of the mamillae and in invasive carcinoma of the breast. Breast Cancer Res. 2004;7(1):R1–R11. doi:10.1186/bcr940.
  • Piana AF, Sotgiu G, Muroni MR, Cossu-Rocca P, Castiglia P, De Miglio MR. HPV infection and triple-negative breast cancers: an Italian case-control study. Virol J. 2014;11(1):190. doi:10.1186/s12985-014-0190-3.
  • Lawson JS, Glenn WK, Salyakina D, Delprado W, Clay R, Antonsson A, Heng B, Miyauchi S, Tran DD, Ngan CC, et al. Human papilloma viruses and breast cancer. Front Oncol. 2015;5:277. doi:10.3389/fonc.2015.00277.
  • Islam S, Dasgupta H, Roychowdhury A, Bhattacharya R, Mukherjee N, Roy A, Mandal GK, Alam N, Biswas J, Mandal S, et al. Study of association and molecular analysis of human papillomavirus in breast cancer of Indian patients: clinical and prognostic implication. PLOS ONE. 2017;12(2):e0172760. doi:10.1371/journal.pone.0172760.
  • Habyarimana T, Attaleb M, Mazarati JB, Bakri Y, El Mzibri M. Detection of human papillomavirus DNA in tumors from Rwandese breast cancer patients. Breast Cancer. 2018;25(2):127–33. doi:10.1007/s12282-018-0831-2.
  • Pajtler M, Audy-Jurković S, Kardum-Skelin I, Mahovlić V, Mozetic-Vrdoljak D, Ovanin-Rakić A. Organisation of cervical cytology screening in Croatia: past, present and future. Coll Antropol. 2007;31:47–54.
  • Kovacevic G, Milosevic V, Knezevic P, Knezevic A, Knezevic I, Radovanov J, Nikolic N, Patic A, Petrovic V, Hrnjakovic Cvjetkovic I, et al. Prevalence of oncogenic Human papillomavirus and genetic diversity in the L1 gene of HPV16 HPV 18 HPV31 and HPV33 found in women from Vojvodina Province Serbia. Biologicals. 2019;58:57–63. doi:10.1016/j.biologicals.2019.02.001.
  • Bruni L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, et al. ICO/IARC information centre on HPV and cancer (HPV information centre). human papillomavirus and related diseases in Croatia. HPV Information Centre; 2019.
  • Yu Y, Morimoto T, Sasa M, Okazaki K, Harada Y, Fujiwara T, Irie Y, Takahashi E-I, Tanigami A, Izumi K, et al. Human papillomavirus type 33 DNA in breast cancer in Chinese. Breast Cancer. 2000;7(1):33–36. doi:10.1007/BF02967185.
  • Wang T, Chang P, Wang L, Yao Q, Guo W, Chen J, Yan T, Cao C. The role of human papillomavirus infection in breast cancer. Med Oncol. 2012;29(1):48–55. doi:10.1007/s12032-010-9812-9.
  • Bernard H-U, Burk RD, Chen Z, Van Doorslaer K, zur Hausen H, de Villiers E-M. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2010;401(1):70–79. doi:10.1016/j.virol.2010.02.002.
  • Harper DM. Currently approved prophylactic HPV vaccines. Expert Rev Vaccines. 2009;8(12):1663–79. doi:10.1586/erv.09.123.
  • Yasmeen A, Bismar TA, Kandouz M, Foulkes WD, Desprez P-Y, Al Moustafa A-E. E6/E7 of HPV type 16 promotes cell invasion and metastasis of human breast cancer cells. Cell Cycle. 2007;6(16):2038–42. doi:10.4161/cc.6.16.4555.
  • Glenn WK, Heng B, Delprado W, Iacopetta B, Whitaker NJ, Lawson JS, Mahieux R. Epstein-Barr virus, human papillomavirus and mouse mammary tumour virus as multiple viruses in breast cancer. PLoS One. 2012;7(11):e48788. doi:10.1371/journal.pone.0048788.
  • Joshi D, Quadri M, Gangane N, Joshi R, Gangane N, Kashanchi F. Association of Epstein Barr virus infection (EBV) with breast cancer in rural Indian women. PLoS One. 2009;4(12):e8180. doi:10.1371/journal.pone.0008180.
  • Lorenzetti MA, De Matteo E, Gass H, Martinez Vazquez P, Lara J, Gonzalez P, Preciado MV, Chabay PA. Characterization of Epstein Barr virus latency pattern in Argentine breast carcinoma. PLoS One. 2010;5(10):e13603. doi:10.1371/journal.pone.0013603.
  • Fawzy S, Sallam M, Awad NM. Detection of Epstein–Barr virus in breast carcinoma in Egyptian women. Clin Biochem. 2008;41(7–8):486–92. doi:10.1016/j.clinbiochem.2007.12.017.
  • Xue SA, Lampert IA, Haldane JS, Bridger JE, Griffin BE. Epstein–Barr virus gene expression in human breast cancer: protagonist or passenger? Br J Cancer. 2003;89(1):113–19. doi:10.1038/sj.bjc.6601027.
  • Zekri ARN, Bahnassy AA, Mohamed WS, El-Kassem FA, El-Khalidi SJ, Hafez MM, Hassan ZK. Epstein-Barr virus and breast cancer: epidemiological and Molecular study on Egyptian and Iraqi women. J Egypt Natl Canc Inst. 2012;24(3):123–31. doi:10.1016/j.jnci.2012.06.001.
  • Iezzoni JC, Gaffey MJ, Weiss LM. The role of Epstein-Barr virus in lymphoepithelioma-like carcinomas. Am J Clin Pathol. 1995;103(3):308–15. doi:10.1093/ajcp/103.3.308.
  • Chu J-S, Chen -C-C, Chang K-J. In situ detection of Epstein–Barr virus in breast cancer. Cancer Lett. 1998;124(1):53–57. doi:10.1016/S0304-3835(97)00449-7.
  • Labrecque LG, Barnes DM, Fentiman IS, Griffin BE. Epstein-Barr virus in epithelial cell tumors: a breast cancer study. Cancer Res. 1995;55:39–45.
  • Luqmani Y, Shousha S. Presence of Epstein-Barr-virus in breast-carcinoma. Int J Oncol. 1995;6:899–903.
  • Bonnet M, Guinebretiere J-M, Kremmer E, Grunewald V, Benhamou E, Contesso G, Joab I. Detection of Epstein-Barr virus in invasive breast cancers. J Natl Cancer Inst. 1999;91(16):1376–81. doi:10.1093/jnci/91.16.1376.
  • Ayee R, Ofori MEO, Wright E, Quaye O. Epstein Barr virus associated lymphomas and epithelia cancers in humans. J Cancer. 2020;11(7):1737–50. doi:10.7150/jca.37282.
  • Kieff EDRA. Epstein-Barr virus and its replication. In: Knipe DMHP, editor. Fields Virology. Philadelphia (USA): Lippincott Williams & Wilkins; 2007. p. 2603–54.
  • Ambinder R, Weiss L. Association of Epstein-Barr virus with Hodgkin’s disease. In: Mauch P, Armitage J, Diehl V, Hoppe R, Weiss L, editors. Hodgkin’s disease. Philadelphia (USA): Lippincott Williams & Wilkins; 1999. p. 79–98.
  • Ballard A. Epstein-Barr virus is associated with aggressive subtypes of invasive ductal carcinoma of breast (Her2+/ER- and triple negative) and with nuclear Expression of NF?B p50. Arch Breast Cancer. 2018;5:68–75.
  • Mazouni C, Fina F, Romain S, Ouafik L, Bonnier P, Martin P-M. Outcome of Epstein-Barr virus-associated primary breast cancer. Mol Clin Oncol. 2015;3(2):295–98. doi:10.3892/mco.2014.459.
  • Corbex M, Bouzbid S, Traverse-Glehen A, Aouras H, McKay-Chopin S, Carreira C, Lankar A, Tommasino M, Gheit T, et al. Prevalence of papillomaviruses, polyomaviruses, and herpesviruses in triple-negative and inflammatory breast tumors from Algeria compared with other types of breast cancer tumors. PLOS ONE. 2014;9(12):e114559. doi:10.1371/journal.pone.0114559.
  • Fessahaye G, Elhassan AM, Elamin EM, Adam AAM, Ghebremedhin A, Ibrahim ME. Association of Epstein - Barr virus and breast cancer in Eritrea. Infect Agent Cancer. 2017;12(1):62. doi:10.1186/s13027-017-0173-2.
  • Wang F-L, Zhang X-L, Yang M, Lin J, Yue Y-F, Li Y-D, Wang X, Shu Q, Jin H-C. Prevalence and characteristics of mouse mammary tumor virus-like virus associated breast cancer in China. Infect Agent Cancer. 2021;16(1):47. doi:10.1186/s13027-021-00383-2.
  • de Sousa Pereira N, Akelinghton Freire Vitiello G, Karina Banin-Hirata B, Scantamburlo Alves Fernandes G, José Sparça Salles M, Karine Amarante M, Angelica Ehara Watanabe M. Mouse Mammary Tumor Virus (MMTV)-like env sequence in Brazilian breast cancer samples: implications in clinicopathological parameters in molecular subtypes. Int J Environ Res Public Health. 2020;17(24):9496. doi:10.3390/ijerph17249496.
  • Slaoui M, El Mzibri M, Razine R, Qmichou Z, Attaleb M, Amrani M. Detection of MMTV-Like sequences in Moroccan breast cancer cases. Infect Agent Cancer. 2014;9(1):37. doi:10.1186/1750-9378-9-37.
  • Hachana M, Trimeche M, Ziadi S, Amara K, Gaddas N, Mokni M, Korbi S. Prevalence and characteristics of the MMTV-like associated breast carcinomas in Tunisia. Cancer Lett. 2008;271(2):222–30. doi:10.1016/j.canlet.2008.06.001.
  • Luo T, Wu XT, Zhang MM, Qian K. Study of mouse mammary tumor virus-like gene sequences expressing in breast tumors of Chinese women. Sichuan Da Xue Xue Bao Yi Xue Ban. 2006;37:51.
  • Levine PH, Pogo BGT, Klouj A, Coronel S, Woodson K, Melana SM, Mourali N, Holland JF. Increasing evidence for a human breast carcinoma virus with geographic differences. Cancer. 2004;101(4):721–26. doi:10.1002/cncr.20436.
  • Ford CE, Tran D, Deng Y, Ta VT, Rawlinson WD, Lawson JS. Mouse mammary tumor virus-like gene sequences in breast tumors of Australian and Vietnamese women. Clin. Cancer Res 2003;9:1118–20.
  • Melana SM, Picconi MA, Rossi C, Mural J, Alonio LV, Teyssié A, et al. Detection of murine mammary tumor virus (MMTV) env gene-like sequences in breast cancer from Argentine patients. Medicina (B Aires). 2002;62:323–27.
  • Etkind P, Du J, Khan A, Pillitteri J, Wiernik PH. Mouse mammary tumor virus-like ENV gene sequences in human breast tumors and in a lymphoma of a breast cancer patient. Clin. Cancer Res 2000;6:1273–78.
  • Pogo BG-T, Melana SM, Holland JF, Mandeli JF, Pilotti S, Casalini P, et al. Sequences homologous to the mouse mammary tumor virus env gene in human breast carcinoma correlate with overexpression of laminin receptor. Clin. Cancer Res 1999;5:2108–11.
  • Wang Y, Holland JF, Bleiweiss IJ, Melana S, Liu X, Pelisson I, et al. Detection of mammary tumor virus ENV gene-like sequences in human breast cancer. Cancer Res. 1995;55:5173–79.
  • Liu B, Wang Y, Melana SM, Pelisson I, Najfeld V, Holland JF, et al. Identification of a Proviral Structure in Human Breast Cancer. Cancer Res. 2001;61:1754–59.
  • Wang Y, Pelisson I, Melana SM, Go V, Holland JF, Pogo BG. MMTV-like env gene sequences in human breast cancer. Arch Virol. 2001;146(1):171–80. doi:10.1007/s007050170201.
  • Loutfy S, Abdallah Z, Shaalan M, Moneer M, Karam A, Moneer M, Sayed IM, Abd El-Hafeez AA, Ghosh P, Zekri ARN, et al. Prevalence of MMTV-like ENV sequences and its association with BRCA1/2 genes mutations among Egyptian breast cancer patients. Cancer Manag Res. 2021;13:2835–48. doi:10.2147/CMAR.S294584.
  • Fukuoka H, Moriuchi M, Yano H, Nagayasu T, Moriuchi H. No association of mouse mammary tumor virus-related retrovirus with Japanese cases of breast cancer. J Med Virol. 2008;80(8):1447–51. doi:10.1002/jmv.21247.
  • Ahangar Oskouee M, Shahmahmoodi S, Jalilvand S, Mahmoodi M, Ziaee AA, Esmaeili HA, Mokhtari-Azad T, Yousefi M, Mollaei-Kandelous Y, Nategh R, et al. No evidence of mammary tumor virus env gene-like sequences among Iranian women with breast cancer. Intervirology. 2014;57(6):353–56. doi:10.1159/000366280.
  • Al Moustafa A-E, Chen D, Ghabreau L, Akil N. Association between human papillomavirus and Epstein-Barr virus infections in human oral carcinogenesis. Med Hypotheses. 2009;73(2):184–86. doi:10.1016/j.mehy.2009.02.025.
  • Lawson JS, Glenn WK. Multiple oncogenic viruses are present in human breast tissues before development of virus associated breast cancer. Infect Agent Cancer. 2017;12(1):55. doi:10.1186/s13027-017-0165-2.
  • Horakova D, Bouchalova K, Cwiertka K, Stepanek L, Vlckova J, Kollarova H. Risks and protective factors for triple negative breast cancer with a focus on micronutrients and infections. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2018;162(2):83–89. doi:10.5507/bp.2018.014.
  • Wang F, Hou J, Shen Q, Yue Y, Xie F, Wang X, et al. Mouse mammary tumor virus-like virus infection and the risk of human breast cancer: a meta-analysis. Am J Transl Res. 2014;6:248–66.
  • Varn FS, Schaafsma E, Wang Y, Cheng C. Genomic characterization of six virus-associated cancers identifies changes in the tumor immune microenvironment and altered genetic programs. Cancer Res. 2018;78(22):6413–23. doi:10.1158/0008-5472.CAN-18-1342.
  • Nik-Zainal S, Alexandrov Ludmil B, Wedge David C, Van Loo P, Greenman Christopher D, Raine K, Jones D, Hinton J, Marshall J, Stebbings L, et al. Mutational processes molding the genomes of 21 breast cancers. Cell. 2012;149(5):979–93. doi:10.1016/j.cell.2012.04.024.
  • Smid M, Rodríguez-González FG, Sieuwerts AM, Salgado R, Prager-Van der Smissen WJC, Vlugt-Daane M, Van Galen A, Nik-Zainal S, Staaf J, Brinkman AB, et al. Breast cancer genome and transcriptome integration implicates specific mutational signatures with immune cell infiltration. Nat Commun. 2016;7(1):12910. doi:10.1038/ncomms12910.
  • Vernet-Tomas M, Mena M, Alemany L, Bravo I, De Sanjosé S, Nicolau P, et al. Human papillomavirus and breast cancer: no evidence of association in a Spanish set of cases. Anticancer Res. 2015;35:851–56.