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Human papillomavirus prevalence and breast carcinogenesis: a systematic review and meta-analysis of published literature

  • K. Favere1
  • S. Menon2
  • K. Valentine2
  • J. Bogers3,4,5
  • D. Vanden Broeck3,4,5,*,

1Faculty of Medicine and Health Sciences, Ghent University, Ghent

2International Centre for Reproductive Health, Ghent University, Ghent

3Applied Molecular Biology Research Group, University of Antwerp, Antwerp

4AML-Molecular Diagnostics, Antwerp

5International Centre for Reproductive Health, Ghent University, Ghent (Belgium)

DOI: 10.12892/ejgo4068.2018 Vol.39,Issue 2,April 2018 pp.161-173

Published: 10 April 2018

*Corresponding Author(s): D. Vanden Broeck E-mail: davy.vandenbroeck@ugent.be

Abstract

Purpose of investigation: The association between human papillomavirus (HPV) infection and breast cancer remains inconclusive as detection rates of high-risk HPV in breast cancer samples are extremely variable. A meta-analysis was conducted to determine the prevalence of HPV in breast neoplasms, with emphasis on genotype distribution. Materials and Methods: A systematic literature search of MEDLINE, The Cochrane Library, and ISI Web of Science databases was conducted, ending in August 2016. A meta-analysis was performed applying the random-effects model. Sub-analyses allowed to estimate the impact of different variables on the pooled prevalence. Results: Forty studies, representing 4762 breast cancer cases, were included. The pooled prevalence of HPV in breast cancer tissue was 20% (95% confidence interval (CI) [12%;29%]). HPV prevalence in breast neoplasms varied by publication period, continental region, HPV primer design, and HPV oncogenic features. Continental region of origin determined the prevailing genotype. Conclusion: The high prevalence of HPV in breast cancer supports the hypothesis that HPV infection is involved in breast carcinogenesis.

Keywords

Breast neoplasms; Review; Meta-analysis; Epidemiology; Etiology; Papillomaviridae.

Cite and Share

K. Favere,S. Menon,K. Valentine,J. Bogers,D. Vanden Broeck. Human papillomavirus prevalence and breast carcinogenesis: a systematic review and meta-analysis of published literature. European Journal of Gynaecological Oncology. 2018. 39(2);161-173.

References

[1] Benson J.R., Jatoi I.: “The global breast cancer burden”. Future Oncol., 2012, 8, 697.

[2] Cancer Research U.K.: “Worldwide cancer incidence statistics 2012” Available at: http://www.cancerresearchuk.org/cancer-info/cancerstats/world/incidence/#Common.

[3] Dumitrescu R.G., Cotarla I.: “Understanding breast cancer risk — where do we stand in 2005?”. J. Cell. Mol. Med., 2005, 9, 208.

[4] Liang W., Wang J., Wang C., Lv Y., Gao H., Zhang K., et al.: “Detection of high-risk human papillomaviruses in fresh breast cancer samples using the hybrid capture 2 assay”. J. Med. Virol., 2013, 85, 2087.

[5] Coughlin S.S., Ekwueme D.U.: “Breast cancer as a global health concern”. Cancer Epidemiol., 2009, 33, 315.

[6] Mou X., Chen L., Liu F., Shen Y., Wang H., Li Y., et al.: “Low prevalence of human papillomavirus (HPV) in Chinese patients with breast cancer”. J. Int. Med. Res., 2011, 39, 1636.

[7] Silva R.G., Jr., da Silva B.B.: “No evidence for an association of human papillomavirus and breast carcinoma”. Breast Cancer Res. Treat., 2011, 125, 261.

[8] de Cremoux P., Thioux M., Lebigot I., Sigal-Zafrani B., Salmon R., Sastre-Garau X., et al.: “No evidence of human papillomavirus DNA sequences in invasive breast carcinoma”. Breast Cancer Res. Treat., 2008, 109, 55.

[9] Band V., Zajchowski D., Kulesa V., Sager R.: “Human papilloma virus DNAs immortalize normal human mammary epithelial cells and reduce their growth factor requirements”. Proc. Natl. Acad. Sci. U.S.A., 1990, 87, 463.

[10] Wazer D.E., Liu X.L., Chu Q., Gao Q., Band V.: “Immortalization of distinct human mammary epithelial cell types by human papilloma virus 16 E6 or E7”. Proc. Natl. Acad. Sci. U.S.A., 1995, 92, 3687.

[11] Di Lonardo A., Venuti A., Marcante M.L.: “Human papillomavirus in breast cancer”. Breast Cancer Res. Treat., 1992, 21, 95.

[12] Bratthauer G.L., Tavassoli F.A., O’Leary T.J.: “Etiology of breast carcinoma: no apparent role for papillomavirus types 6/11/16/18”. Pathol. Res. Pract., 1992, 188, 384.

[13] Wrede D., Luqmani Y.A., Coombes R.C., Vousden K.H.: “Absence of HPV 16 and 18 DNA in breast cancer”. Br. J. Cancer, 1992, 65, 891.

[14] Gopalkrishna V., Singh U.R., Sodhani P., Sharma J.K., Hedau S.T., Mandal A.K., et al.: “Absence of human papillomavirus DNA in breast cancer as revealed by polymerase chain reaction”. Breast Cancer Res. Treat., 1996, 39, 197.

[15] Lindel K., Forster A., Altermatt H.J., Greiner R., Gruber G.: “Breast cancer and human papillomavirus (HPV) infection: no evidence of a viral etiology in a group of Swiss women”. Breast, 2007, 16, 172.

[16] Antonsson A., Spurr T.P., Chen A.C., Francis G.D., McMillan N.A., Saunders N.A., et al.: “High prevalence of human papillomaviruses in fresh frozen breast cancer samples”. J. Med. Virol., 2011, 83, 2157.

[17] Gumus M., Yumuk P.F., Salepci T., Aliustaoglu M., Dane F., Ekenel M., et al.: “HPV DNA frequency and subset analysis in human breast cancer patients’ normal and tumoral tissue samples”. J. Exp. Clin. Cancer Res., 2006, 25, 515.

[18] Bae J.M., Kim E.H.: “Human papillomavirus infection and risk of breast cancer: a meta-analysis of case-control studies”. Infect. Agent. Cancer, 2016, 11, 14.

[19] Lawson J.S., Glenn W.K., Heng B., Ye Y., Tran B., Lutze-Mann L., et al.: “Koilocytes indicate a role for human papilloma virus in breast cancer”. Br. J. Cancer., 2009, 101, 1351.

[20] Lawson J.S., Glenn W.K., Salyakina D., Delprado W., Clay R., Antonsson A., et al.: “Human Papilloma Viruses and Breast Cancer”. Front. Oncol., 2015, 5, 277.

[21] Li N., Bi X., Zhang Y., Zhao P., Zheng T., Dai M.: “Human papillomavirus infection and sporadic breast carcinoma risk: a meta-analysis”. Breast Cancer Res. Treat., 2011, 126, 515.

[22] Stroup D.F., Berlin J.A., Morton S.C., Olkin I., Williamson G.D., Rennie D., et al.: “Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group”. JAMA, 2000, 283, 2008.

[23] Moher D., Liberati A., Tetzlaff J., Altman D.G., Group P.: “Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement”. Ann. Intern. Med., 2009, 151, 264.

[24] Yu Y., Morimoto T., Sasa M., Okazaki K., Harada Y., Fujiwara T., et al.: “HPV33 DNA in premalignant and malignant breast lesions in Chinese and Japanese populations”. Anticancer Res., 1999, 19, 5057.

[25] Yu Y., Morimoto T., Sasa M., Okazaki K., Harada Y., Fujiwara T., et al.: “Human papillomavirus type 33 DNA in breast cancer in Chinese”. Breast Cancer, 2000, 7, 33.

[26] Kulka J., Kovalszky I., Svastics E., Berta M., Fule T.: “Lymphoepithelioma-like carcinoma of the breast: not Epstein-Barr virus-, but human papilloma virus-positive”. Hum. Pathol., 2008, 39, 298.

[27] Czerwenka K., Heuss F., Hosmann J.W., Manavi M., Lu Y., Jelincic D., et al.: “Human papilloma virus DNA: a factor in the pathogenesis of mammary Paget’s disease?” Breast Cancer Res. Treat., 1996, 41, 51.

[28] Grenier J., Soria J.C., Mathieu M.C., Andre F., Abdelmoula S., Velasco V., et al.: “Differential immunohistochemical and biological profile of squamous cell carcinoma of the breast”. Anticancer Res., 2007, 27, 547.

[29] Aceto G.M., Solano A.R., Neuman M.I., Veschi S., Morgano A., Malatesta S., et al.: “High-risk human papilloma virus infection, tumor pathophenotypes, and BRCA1/2 and TP53 status in juvenile breast cancer”. Breast Cancer Res. Treat., 2010, 122, 671.

[30] Widschwendter A., Brunhuber T., Wiedemair A., Mueller-Holzner E., Marth C.: “Detection of human papillomavirus DNA in breast cancer of patients with cervical cancer history”. J. Clin. Virol., 2004, 31, 292.

[31] Hennig E.M., Suo Z., Thoresen S., Holm R., Kvinnsland S., Nesland J.M.: “Human papillomavirus 16 in breast cancer of women treated for high grade cervical intraepithelial neoplasia (CIN III)”. Breast Cancer Res. Treat., 1999, 53, 121.

[32] Lawson J.S., Glenn W.K., Salyakina D., Clay R., Delprado W., Cheerala B., et al.: “Human Papilloma Virus Identification in Breast Cancer Patients with Previous Cervical Neoplasia”. Front. Oncol., 2015, 5, 298.

[33] Mohtasebi P., Rassi H., Maleki F., Hajimohammadi S., Bagheri Z., Fakhar Miandoab M., et al.: “Detection of Human Papillomavirus Genotypes and Major BRCA Mutations in Familial Breast Cancer”. Monoclon. Antib. Immunodiagn. Immunother., 2016, 35, 135.

[34] United Nations Statistics Division: “Composition of macro geographical (continental) regions, geographical sub-regions, and selected economic and other groupings 2012”. Available at: http://unstats.un.org/unsd/methods/m49/m49regin.htm.

[35] Munoz N., Bosch F.X., de Sanjose S., Herrero R., Castellsague X., Shah K.V., et al.: “Epidemiologic classification of human papillomavirus types associated with cervical cancer”. N. Engl. J. Med., 2003, 348, 518.

[36] El-Shinawi M., Mohamed H.T., Abdel-Fattah H.H., Ibrahim S.A., El-Halawany M.S., Nouh M.A., et al.: “Inflammatory and Non-inflammatory Breast Cancer: A Potential Role for Detection of Multiple Viral DNAs in Disease Progression”. Ann. Surg. Oncol., 2016. 23, 494.

[37] 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.

[38] Salehpour M., Tayyebi Meibodi N., Teimourpour R., Ghorani-Azam A., Sepahi S., Rostami S., et al.: “Frequency of Human Papillomavirus Genotypes 6, 11, 16, 18 And 31 in Paraffin-Embedded Tissue Samples of Invasive Breast Carcinoma, North- East of Iran”. Iran. J. Pathol., 2015, 10, 192.

[39] Vernet-Tomas M., Mena M., Alemany L., Bravo I., De Sanjose 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.

[40] Ngan C., Lawson J.S., Clay R., Delprado W., Whitaker N.J., Glenn W.K.: “Early Human Papilloma Virus (HPV) Oncogenic Influences in Breast Cancer”. Breast Cancer (Auckl.), 2015, 9, 93.

[41] Piana A.F., Sotgiu G., Muroni M.R., Cossu-Rocca P., Castiglia P., De Miglio M.R.: “HPV infection and triple-negative breast cancers: an Italian case-control study”. Virol. J., 2014, 11, 190.

[42] Ohba K., Ichiyama K., Yajima M., Gemma N., Nikaido M., Wu Q., et al.: “In vivo and in vitro studies suggest a possible involvement of HPV infection in the early stage of breast carcinogenesis via APOBEC3B induction”. PLoS One, 2014, 9, e97787.

[43] Wang T., Zeng X., Li W., Zhu H., Wang G., Liu X., et al.: “Detection and analysis of human papillomavirus (HPV) DNA in breast cancer patients by an effective method of HPV capture”. PLoS One, 2014, 9, e90343.

[44] Corbex M., Bouzbid S., Traverse-Glehen A., Aouras H., McKayChopin S., Carreira C., 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, e114559.

[45] Lv Y.R., Wang J.L., Zhang K., Gao H.D., Sun J.Z., Gong Y.Y., et al.: “Human Papilloma Viruses (HPVs) no Co-Existence in Breast Cancer and Cervical Cells in the Same Patient”. Chinese J. Physiol., 2014, 57, 105.

[46] Moradi A.M., E.; Tabarraei, A.; Bakhshandeh Nosrat, S.; Kazemi nejad, V.; Azarhosh, R.; Alizadeh, S; Bazori, M.;. “Molecular epidemiology of Human Papillomaviruses in breast cancer, Golestan province of Iran”. Medical Laboratory Journal, 2009, 3.

[47] Fernandes A., Bianchi G., Feltri A.P., Perez M., Correnti M.: “Presence of human papillomavirus in breast cancer and its association with prognostic factors”. Ecancermedicalscience, 2015, 9, 548.

[48] Pereira Suarez A.L., Lorenzetti M.A., Gonzalez Lucano R., Cohen M., Gass H., Martinez Vazquez P., et al.: “Presence of human papilloma virus in a series of breast carcinoma from Argentina”. PLoS One, 2013, 8, e61613.

[49] Hossein R., Behzad S., Tahar M., Azadeh N.A.: “Prevalence of human papillomavirus genotypes associated with cervical and breast cancers in iran”. Monoclon. Antib. Immunodiagn. Immunother., 2013, 32, 399.

[50] Herrera-Goepfert R., Vela-Chavez T., Carrillo-Garcia A., LizanoSoberon M., Amador-Molina A., Onate-Ocana L.F., et al.: “Highrisk human papillomavirus (HPV) DNA sequences in metaplastic breast carcinomas of Mexican women”. BMC Cancer, 2013, 13, 445.

[51] Khoury J.D., Tannir N.M., Williams M.D., Chen Y., Yao H., Zhang J., et al.: “Landscape of DNA virus associations across human malignant cancers: analysis of 3,775 cases using RNA-Seq”. J. Virol., 2013, 87, 8916.

[52] Herrera-Romano L., Fernandez-Tamayo N., Gomez-Conde E., Reyes-Cardoso J.M., Ortiz-Gutierrez F., Ceballos G., et al.: “Absence of human papillomavirus sequences in epithelial breast cancer in a Mexican female population”. Med. Oncol., 2012, 29, 1515.

[53] Baltzell K., Buehring G.C., Krishnamurthy S., Kuerer H., Shen H.M., Sison J.D.: “Limited evidence of human papillomavirus in [corrected] breast tissue using molecular in situ methods”. Cancer, 2012, 118, 1212.

[54] Hedau S., Kumar U., Hussain S., Shukla S., Pande S., Jain N., et al.: “Breast cancer and human papillomavirus infection: no evidence of HPV etiology of breast cancer in Indian women”. BMC Cancer, 2011, 11, 27.

[55] Aguayo F., Khan N., Koriyama C., Gonzalez C., Ampuero S., Padilla O., et al.: “Human papillomavirus and Epstein-Barr virus infections in breast cancer from chile”. Infect. Agent. Cancer, 2011, 6, 7.

[56] Ghaffari S.R., Sabokbar T., Meshkat Z., Fereidooni F., Dastan J., Rafati M., et al.: “Tracing human papilloma virus in breast tumors of Iranian breast cancer patients”. Breast J., 2011, 17, 218.

[57] Hachana M., Ziadi S., Amara K., Toumi I., Korbi S., Trimeche M.: “No evidence of human papillomavirus DNA in breast carcinoma in Tunisian patients”. Breast, 2010, 19, 541.

[58] Ong K., Koay E.S., Putti T.C.: “Detection of cutaneous HPV types 4 and 24 DNA sequences in breast carcinoma in Singaporean women of Asian ancestry”. Pathology, 2009, 41, 436.

[59] Akil N., Yasmeen A., Kassab A., Ghabreau L., Darnel A.D., 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, 404.

[60] Duo D., Ghimenti C., Migliora P., Pavanelli M.C., Mastracci L., Angeli G.: “Identification and characterization of human papillomavirus DNA sequences in Italian breast cancer patients by PCR and line probe assay reverse hybridization”. Mol. Med. Rep., 2008, 1, 673.

[61] Kroupis C., Markou A., Vourlidis N., Dionyssiou-Asteriou A., Lianidou E.S.: “Presence of high-risk human papillomavirus sequences in breast cancer tissues and association with histopathological characteristics”. Clin. Biochem., 2006, 39, 727.

[62] Kan C.Y., Iacopetta B.J., Lawson J.S., Whitaker N.J.: “Identification of human papillomavirus DNA gene sequences in human breast cancer”. Br. J. Cancer, 2005, 93, 946.

[63] de Villiers E.M., Sandstrom R.E., zur Hausen H., Buck C.E.: “Presence of papillomavirus sequences in condylomatous lesions of the mamillae and in invasive carcinoma of the breast”. Breast Cancer Res, 2005, 7, R1.

[64] Li T., Lu Z.M., Guo M., Wu Q.J., Chen K.N., Xing H.P., et al.: “p53 codon 72 polymorphism (C/G) and the risk of human papillomavirus-associated carcinomas in China”. Cancer, 2002, 95, 2571.

[65] Liu Y., Klimberg V.S., Andrews N.R., Hicks C.R., Peng H., ChirivaInternati M., et al.: “Human papillomavirus DNA is present in a subset of unselected breast cancers”. J. Hum. Virol., 2001, 4, 329.

[66] Zhou Y., Li J., Ji Y., Ren M., Pang B., Chu M., et al.: “Inconclusive role of human papillomavirus infection in breast cancer”. Infect. Agent. Cancer, 2015, 10, 36.

[67] Higgins J.P.T., Green S.: “Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0”. The Cochrane Collaboration, 2011. Available at: http://handbook.cochrane.org.

[68] Nyaga V.N., Arbyn M., Aerts M.: “Metaprop: a Stata command to perform meta-analysis of binomial data”. Arch. Public Health, 2014, 72.

[69] Simoes P.W., Medeiros L.R., Pires P.D.S., Edelweiss M.I., Rosa D.D., Silva F.R., et al.: “Prevalence of Human Papillomavirus in Breast Cancer A Systematic Review”. International Journal of Gynecological Cancer, 2012, 22, 343.

[70] Wang T., Chang P., Wang L., Yao Q., Guo W., Chen J., et al.: “The role of human papillomavirus infection in breast cancer”. Med. Oncol., 2012, 29, 48.

[71] Akarolo-Anthony S.N., Famooto A.O., Dareng E.O., Olaniyan O.B., Offiong R., Wheeler C.M., et al.: “Age-specific prevalence of human papilloma virus infection among Nigerian women”. BMC Public Health, 2014, 14, 656.

[72] Girianelli V.R., Thuler L.C., e Silva G.A.: “[Prevalence of HPV infection among women covered by the family health program in the Baixada Fluminense, Rio de Janeiro, Brazil]”. Rev. Bras. Ginecol. Obstet., 2010, 32, 39.

[73] Bruni L., Diaz M., Castellsague X., Ferrer E., Bosch F.X., de Sanjose S.: “Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings”J. Infect. Dis., 2010, 202, 1789.

[74] Lawson JS G.W., Whitaker NJ. “Reply: Breast cancer, human papilloma virus and sexual activities”. Br. J. Cancer, 2008, 98, 510.

[75] Damin A.P., Karam R., Zettler C.G., Caleffi M., Alexandre C.O.: “Evidence for an association of human papillomavirus and breast carcinomas”. Breast Cancer Res. Treat., 2004, 84, 131.

[76] Lawson J.S., Kan C.Y., Iacopetta B.J., Whitaker N.J.: “Are some breast cancers sexually transmitted?”. Br. J. Cancer, 2006, 95, 1708.

[77] Khan N.A., Castillo A., Koriyama C., Kijima Y., Umekita Y., Ohi Y., et al.: “Human papillomavirus detected in female breast carcinomas in Japan”. Br. J. Cancer, 2008, 99, 408.

[78] Heng B., Glenn W.K., Ye Y., Tran B., Delprado W., Lutze-Mann L., et al.: “Human papilloma virus is associated with breast cancer”. Br. J. Cancer, 2009, 101, 1345.

[79] Schiffman M., Clifford G., Buonaguro F.M.: “Classification of weakly carcinogenic human papillomavirus types: addressing the limits of epidemiology at the borderline”. Infect. Agent. Cancer, 2009, 4, 8.

[80] Cheng Y.W., Chiou H.L., Sheu G.T., Hsieh L.L., Chen J.T., Chen C.Y., et al.: “The association of human papillomavirus 16/18 infection with lung cancer among nonsmoking Taiwanese women”. Cancer Res., 2001, 61, 2799.

[81] Pao C.C., Lin S.S., Lin C.Y., Maa J.S., Lai C.H., Hsieh T.T.: “Identification of human papillomavirus DNA sequences in peripheral blood mononuclear cells”. Am. J. Clin. Pathol., 1991, 95, 540.

[82] Capone R.B., Pai S.I., Koch W.M., Gillison M.L., Danish H.N., Westra W.H., et al.: “Detection and quantitation of human papillomavirus (HPV) DNA in the sera of patients with HPV-associated head and neck squamous cell carcinoma”. Clin. Cancer Res., 2000, 6, 4171.

[83] Bodaghi S., Wood L.V., Roby G., Ryder C., Steinberg S.M., Zheng Z.M.: “Could human papillomaviruses be spread through blood?“. J. Clin. Microbiol., 2005, 43, 5428.

[84] Joshi D., Buehring G.C.: “Are viruses associated with human breast cancer? Scrutinizing the molecular evidence”. Breast Cancer Res. Treat., 2012, 135, 1.

[85] Skinner G.R.: “Transformation of primary hamster embryo fibroblasts by type 2 simplex virus: evidence for a “hit and run” mechanism”. Br. J. Exp. Pathol., 1976, 57, 361.


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