2,648
Views
21
CrossRef citations to date
0
Altmetric
Research Paper

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

, , , , , , & show all
Pages 982-989 | Received 05 Jun 2020, Accepted 26 Jul 2020, Published online: 02 Oct 2020

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.
  • Narayan AK, Al-Naemi H, Aly A, Kharita MH, Khera RD, Hajaj M, Rehani MM. Breast cancer detection in Qatar: evaluation of mammography image quality using a standardized assessment tool. Eur J Breast Health. 2020;16(2):124–28. doi:10.5152/ejbh.2020.5115.
  • Donnelly TT, Al Khater A-H, Al Kuwari MG, Al-Bader SB, Al-Meer N, Abdulmalik M, Singh R, Chaudhry S, Fung T. Do socioeconomic factors influence breast cancer screening practices among Arab women in Qatar? BMJ Open. 2015;5(1):e005596–e005596. doi:10.1136/bmjopen-2014-005596.
  • Bener A, Ayub H, Kakil R, Ibrahim W. Patterns of cancer incidence among the population of Qatar: a worldwide comparative study. Asian Pac J Cancer Prev. 2008 Apr 29;9(1):19–24.
  • Venuti ABG, 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.
  • Daling JRMM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, Carter JJ, Porter PL, Galloway DA, McDougall JK. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer. Cancer. 2004;101:270–80. doi:10.1002/cncr.20365.
  • Ragin C, 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;121:1813–20. doi:10.1002/ijc.22851.
  • Shi Y, Peng S-L, Yang L-F, Chen X, Tao Y-G, Cao Y. Co-infection of Epstein-Barr virus and human papillomavirus in human tumorigenesis. Chin J Cancer. 2016;35:16–16. doi:10.1186/s40880-016-0079-1.
  • Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: A meta-analysis update. Int J Cancer. 2007;121(3):621–32. doi:10.1002/ijc.22527.
  • Syrjänen KJ. HPV infections and oesophageal cancer. J Clin Pathol. 2002;55(10):721–28. doi:10.1136/jcp.55.10.721.
  • Akil N, Yasmeen A, Kassab A, Ghabreau L, Darnel AD, Al Moustafa AE. 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.
  • Delgado-García S, Martínez-Escoriza JC, 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.
  • Graflund MSB, Sigurdardóttir S, Karlsson M. HPV-DNA, vascular space invasion, and their impact on the clinical outcome in early-stage cervical carcinomas. Int J Gynecol Cancer. 2004;14:896–902. doi:10.1111/j.1048-891X.2004.014527.x.
  • Umudum H, Rezanko T, Dag F, Dogruluk T. Human papillomavirus genome detection by in situ hybridization in fine-needle aspirates of metastatic lesions from head and neck squamous cell carcinomas. Cancer. 2005;105:171–77. doi:10.1002/cncr.21027.
  • Zuna R, Allen RA, Moore WE, Mattu R, Dunn ST. Comparison of human papillomavirus genotypes in high-grade squamous intraepithelial lesions and invasive cervical carcinoma: evidence for differences in biologic potential of precursor lesions. Mod Pathol. 2004;17:1314–22. doi:10.1038/modpathol.3800223.
  • 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.
  • 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.
  • Cyprian FS, Al-Farsi HF, Vranic S, Akhtar S, Al Moustafa A-E. Epstein-barr virus and human papillomaviruses interactions and their roles in the initiation of epithelial-mesenchymal transition and cancer progression. Front Oncol. 2018;8:111–111. 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.
  • 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 Sur Oral Med Oral Pathol Oral Radiol Endodontol. 1995;79(1):57–63. doi:10.1016/S1079-2104(05)80075-7.
  • 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.
  • McCloskey R, Menges C, Friedman A, Patel D, McCance DJ. Human papillomavirus type 16 E6/E7 upregulation of nucleophosmin is important for proliferation and inhibition of differentiation. J Virol. 2010;84(10):5131–39. doi:10.1128/jvi.01965-09.
  • Al Moustafa A, 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;23:350–58. doi:10.1038/sj.onc.1207148.
  • Al Moustafa A, Kassab A, Darnel A, Yasmeen A. High-risk HPV/ErbB-2 interaction on E-cadherin/catenin regulation in human carcinogenesis. Curr Pharm Des. 2008;14:2159–72. doi:10.2174/138161208785740216.
  • Al Moustafa A-E. 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.
  • 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(7):1936–39. doi:10.1080/21645515.2016.1139255.
  • 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.
  • Al Moustafa A-E, Cyprian FS, Al-Antary N, Yasmeen A. High-risk human papillomaviruses and epstein-barr virus presence and crosstalk in human oral carcinogenesis. In: Al Moustafa A-E, editor. Development of oral cancer: risk factors and prevention strategies. Cham, Switzerland: Springer International Publishing; 2017. p. 83–94.
  • 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;8:250–250. doi:10.3389/fonc.2018.00250.
  • 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.
  • Al Moustafa A-E. Role of high-risk human papillomaviruses in breast carcinogenesis. In: Gupta S, editor. Breast carcinogenesis; Oncoviruses and their inhibitors. Boca Raton, Florida: CRC: Taylor and Francis Group; 2014. p. 245–62.
  • 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.
  • Hedau S, Kumar U, Hussain S, Shukla S, Pande S, Jain N, Tyagi A, Deshpande T, Bhat D, Mir MM, et al. Breast cancer and human papillomavirus infection: no evidence of HPV etiology of breast cancer in Indian women. BMC Cancer. 2011;11(1):27. doi:10.1186/1471-2407-11-27.
  • Brumbaugh J, Ferris RL, Hu S. HPV and EBV in head and neck cancer. In: Bernier J, editor. Head and neck cancer: multimodality management. Cham, Switzerland: Springer International Publishing; 2016. p. 163–79.
  • 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. 2020:1–5. doi:10.1080/21645515.2020.1726680.
  • Al-Thawadi H, Gupta I, Jabeen A, Skenderi F, Aboulkassim T, Yasmeen A, Malki MI, Batist G, Vranic S, Al Moustafa A-E. 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;20:1–13. doi:10.1186/s12935-020-01348-y.
  • 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.
  • 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.
  • Gupta I, Nasrallah GK, Sharma A, Jabeen A, Smatti MK, Al-Thawadi HA, Sultan AA, Alkhalaf M, Vranic S, Moustafa AA. Co-prevalence of human papillomaviruses (HPV) and Epstein-Barr virus (EBV) in healthy blood donors from diverse nationalities in Qatar. Cancer Cell Int. 2020;20:107–107. 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.
  • 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.
  • 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;15:53–53. doi:10.1186/s12935-015-0206-0.
  • Zur Hausen H. Papillomaviruses in the causation of human cancers — a brief historical account. Virology. 2009;384(2):260–65. doi:10.1016/j.virol.2008.11.046.
  • 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.
  • Gumus M, Yumuk PF, Salepci T, Aliustaoglu M, Dane F, Ekenel M, Basaran G, Kaya H, Barisik N, Turhal NS, et al. HPV DNA frequency and subset analysis in human breast cancer patients’ normal and tumoral tissue samples. J Exp Clin Cancer Res. 2006 Jan 22;25(4):515–21.
  • Ali SH, Al-Alwan NA, Al-Alwany SH. Detection and genotyping of human papillomavirus in breast cancer tissues from Iraqi patients. East Mediterr Health J. 2014 Jun 25;20(6):372–77. doi:10.26719/2014.20.6.372.
  • Sigaroodi A, Nadji SA, Naghshvar F, Nategh R, Emami H, Velayati AA. Human papillomavirus is associated with breast cancer in the north part of Iran. Sci World J. 2012;2012:837191–837191. doi:10.1100/2012/837191.
  • Ahangar-Oskouee M, Shahmahmoodi S, Jalilvand S, Mahmoodi M, Ziaee AA, Esmaeili H-A, Keshtvarz M, Pishraft-Sabet L, Yousefi M, Mollaei-Kandelous Y, et al. No detection of ‘high-risk’ human papillomaviruses in a group of Iranian women with breast cancer. Asian Pac J Cancer Prev. 2014;15(9):4061–65. doi:10.7314/apjcp.2014.15.9.4061.
  • Manzouri L, Salehi R, Shariatpanahi S, Rezaie P. Prevalence of human papilloma virus among women with breast cancer since 2005–2009 in Isfahan. Adv Biomed Res. 2014;3:75. doi:10.4103/2277-9175.125873.
  • Elmi A, Bansal D, Al-Thani A, Al-Ansari A, Mohamed N, Sultan A. Molecular epidemiology of human papillomavirus among Arab women in Qatar. Qatar Foundation Annual Research Forum Proceedings. 2012;2012(1). doi:10.5339/qfarf.2012.BMP6.
  • Bansal D, Elmi AA, Skariah S, Haddad P, Abu-Raddad LJ, Al Hamadi AH, Mohamed-Nady N, Affifi NM, Ghedira R, Hassen E, et al. Molecular epidemiology and genotype distribution of human papillomavirus (HPV) among Arab women in the state of Qatar. J Transl Med. 2014;12(1):300. doi:10.1186/s12967-014-0300-4.
  • Moosa K, Alsayyad AS, Quint W, Gopala K, DeAntonio R. An epidemiological study assessing the prevalence of human papillomavirus types in women in the Kingdom of Bahrain. BMC Cancer. 2014;14:905–905. doi:10.1186/1471-2407-14-905.
  • AlObaid A, Al-Badawi IA, Al-Kadri H, Gopala K, Kandeil W, Quint W, Al-Aker M, DeAntonio R. Human papillomavirus prevalence and type distribution among women attending routine gynecological examinations in Saudi Arabia. BMC Infect Dis. 2014;14(1):643. doi:10.1186/s12879-014-0643-8.
  • Al-Awadhi R, Chehadeh W, Jaragh M, Al-Shaheen A, Sharma P, Kapila K. Distribution of human papillomavirus among women with abnormal cervical cytology in Kuwait. Diagn Cytopathol. 2013;41(2):107–14. doi:10.1002/dc.21778.
  • 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.
  • 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;5:277–277. doi:10.3389/fonc.2015.00277.
  • 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.
  • De Carolis S, Storci G, Ceccarelli C, Savini C, Gallucci L, Sansone P, Santini D, Seracchioli R, Taffurelli M, Fabbri F, et al. HPV DNA associates with breast cancer malignancy and it is transferred to breast cancer stromal cells by extracellular vesicles. Front Oncol. 2019;9(860). doi:10.3389/fonc.2019.00860
  • Corbex M, Bouzbid S, Traverse-Glehen A, Aouras H, McKay-Chopin S, Carreira C, Lankar A, Tommasino M, Gheit T. 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.
  • 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.
  • Glenn WK, Heng B, Delprado W, Iacopetta B, Whitaker NJ, Lawson JS. Epstein-Barr virus, human papillomavirus and mouse mammary tumour virus as multiple viruses in breast cancer. PloS One. 2012;7(11):e48788–e48788. doi:10.1371/journal.pone.0048788.
  • Joshi D, Quadri M, Gangane N, Joshi R, Gangane N. Association of Epstein Barr virus infection (EBV) with breast cancer in rural Indian women. PloS One. 2009;4(12):e8180–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–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.
  • Kalkan A, Ozdarendeli A, Bulut Y, Yekeler H, Cobanoglu B, Doymaz MZ. Investigation of Epstein-Barr virus DNA in formalin-fixed and paraffin- embedded breast cancer tissues. Med Princ Pract. 2005;14(4):268–71. doi:10.1159/000085748.
  • Aboulkassim T, Yasmeen A, Akil N, Batist G, Al Moustafa A-E. Incidence of Epstein-Barr virus in Syrian women with breast cancer: A tissue microarray study. Hum Vaccin Immunother. 2015;11(4):951–55. doi:10.1080/21645515.2015.1009342.
  • Zekri A-RN, 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 Cancer Inst. 2012;24(3):123–31. doi:10.1016/j.jnci.2012.06.001.
  • Hachana M, Amara K, Ziadi S, Romdhane E, Gacem RB, Trimeche M. Investigation of Epstein-Barr virus in breast carcinomas in Tunisia. Pathol Res Pract. 2011;207(11):695–700. doi:10.1016/j.prp.2011.09.007.
  • Sharifpour C, Makvandi M, Samarbafzadeh A, Talaei-Zadeh A, Ranjbari N, Nisi N, Azaran A, Jalilian S, Varnaseri M, Pirmoradi R, et al. Frequency of Epstein–Barr virus DNA in formalin-fixed paraffin-embedded tissue of patients with ductal breast carcinoma. Asian Pac J Cancer Prev. 2019;20(3):687–92. doi:10.31557/apjcp.2019.20.3.687.
  • Farahmand M, Monavari SH, Shoja Z, Ghaffari H, Tavakoli M, Tavakoli A. Epstein-Barr virus and risk of breast cancer: a systematic review and meta-analysis. Future Oncol. 2019;15(24):2873–85. doi:10.2217/fon-2019-0232.
  • 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.
  • Naushad W, Surriya O, Sadia H. Prevalence of EBV, HPV and MMTV in Pakistani breast cancer patients: A possible etiological role of viruses in breast cancer. Infec Genet Evol. 2017;54:230–37. doi:10.1016/j.meegid.2017.07.010.
  • Fina F, Romain S, Ouafik L, Palmari J, Ayed FB, Benharkat S, Bonnier P, Spyratos F, Foekens JA, Rose C, et al. Frequency and genome load of Epstein-Barr virus in 509 breast cancers from different geographical areas. Br J Cancer. 2001;84(6):783–90. doi:10.1054/bjoc.2000.1672.
  • 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. Biomedical Papers. 2018;162(2):83–89. doi:10.5507/bp.2018.014.
  • Corbex M, Bouzbid S, Boffetta P. Features of breast cancer in developing countries, examples from North-Africa. Eur J Cancer. 2014;50(10):1808–18. doi:10.1016/j.ejca.2014.03.016.
  • Lawson JS, Salmons B, Glenn WK. Oncogenic viruses and breast cancer: mouse mammary tumor virus (MMTV), bovine leukemia virus (BLV), human papilloma virus (HPV), and Epstein-Barr virus (EBV). Front Oncol. 2018;8:1–1. doi:10.3389/fonc.2018.00001.
  • Aguayo F, Khan N, Koriyama C, González C, Ampuero S, Padilla O, Solís L, Eizuru Y, Corvalán A, Akiba S, et al. Human papillomavirus and Epstein-Barr virus infections in breast cancer from chile. Infect Agent Cancer. 2011;6(1):7–7. doi:10.1186/1750-9378-6-7.
  • Gupta I, Al Farsi H, Jabeen A, Skendri F, Al-Thawadi H, AlAhmad YM, Al Moustafa AE, Vranic S. High-risk human papillomaviruses and Epstein-Barr virus in colorectal cancer and their association with clinicopathological status. Pathogens. 2020;9: (In Press). doi:10.3390/pathogens9060452.
  • Gupta I, Jabeen A, Skenderi F, Malki MI, Al-Thawadi H, Al Moustafa AE, Vranic S. High-risk human papillomaviruses (HPV) and Epstein - Barr virus (EBV) are commonly present in rectal cancer. Mod Pathol. 2020;33:676.
  • Gupta I, Ghabreau L, Al-Thawadi H, Yasmeen A, Vranic S, Al Moustafa AE, Malki MI. Co-incidence of human papillomaviruses and Epstein-Barr virus is associated with high to intermediate tumor grade in human head and neck cancer in Syria. Front Oncol. 2020. doi:10.3389/fonc.2020.01016.