Skip to main content

Advertisement

SpringerLink
Log in

Detection of human papillomavirus DNA in tumors from Rwandese breast cancer patients

  • Review Article
  • Published:
Breast Cancer Aims and scope Submit manuscript

Abstract

Background

During the last decades, a great interest was given to viral etiology of breast cancer. Indeed, due to recent technical improvements and some encouraging new results, it has been a resurgence of interest in the possibility that a substantial proportion of human breast cancers may be caused by viral infections. High-risk genotypes of human papillomavirus (HPV) have been found in breast cancer cases. In the present study, we aimed to assess the presence of HPV DNA in breast cancer cases from Rwanda and to evaluate the association between HPV infection and clinico-pathological features.

Methods

Therefore, a total of 47 archived formalin-fixed paraffin-embedded biopsies were collected and complete information was recorded. HPV detection and genotyping were done by PCR amplification and DNA sequencing.

Results

Overall, HPV DNA was found in 46.81% of cases, HPV16 being the most prevalent subtype (77.27%) followed by HPV33 (13.64%) and HPV31 (9.09%). Comparison of HPV with clinico-pathological features showed no significant difference between HPV infection and breast localization, histological subtype, clinical stage, tumor grade, and intrinsic molecular subtypes.

Conclusions

These findings provide evidence of high prevalence of high-risk HPV in Rwandese patients with breast cancer and suggest that high-risk HPV infections could be a risk factor associated with human breast cancer development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kantelhardt EJ, Cubasch H, Hanson C. Taking on breast cancer in East Africa: global challenges in breast cancer. Curr Opin Obstet Gynecol. 2015;27:108–14. https://doi.org/10.1097/GCO.0000000000000139.

    Article  Google Scholar 

  2. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C et al. GLOBOCAN 2012 v1.0, Cancer incidence and mortality worldwide: IARC Cancer base no. 11 [Internet]. Lyon: International Agency for Research on Cancer. 2013. http://globocan.iarc.fr.

  3. Ferlay J, Shin H-R, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. I. Int J Cancer. 2010;127(12):2893–917. https://doi.org/10.1002/ijc.25516.

    Article  CAS  Google Scholar 

  4. Jung SJ, Song M, Choi JY, Song N, Park SK, Yoo KY, et al. Association of selected medical conditions with breast cancer risk in Korea. J Prev Med Public Health. 2013;46:346–52. https://doi.org/10.3961/jpmph.2013.46.6.346.

    Article  Google Scholar 

  5. Stewart BW, Kleihues P. World cancer report. Lyon: IARC Press; 2003.

    Google Scholar 

  6. Amarante MK, Watanabe MAE. The possible involvement of virus in breast cancer. J Cancer Res Clin Oncol. 2009;135:329–37. https://doi.org/10.1007/s00432-008-0511-2.

    Article  Google Scholar 

  7. 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(3):248–66.

    PubMed  PubMed Central  Google Scholar 

  8. Huo Q, Zhang N, Yang Q. Epstein–Barr virus infection and sporadic breast cancer risk: a meta-analysis. PLoS One. 2012;7(2):e31656. https://doi.org/10.1371/journal.pone.0031656.

    Article  CAS  Google Scholar 

  9. Bae J-M, Kim EH. Human papillomavirus infection and risk of breast cancer: a meta-analysis of case- control studies. Infect Agents Cancer. 2016;11:14. https://doi.org/10.1186/s13027-016-0058-9.

    Article  Google Scholar 

  10. Damin APS, Karam R, Zettler CG, Caleffi M, Alexandre COP. Evidence for an association of human papillomavirus and breast carcinomas. Breast Cancer Res Treat. 2004;84:131–7.

    Article  CAS  PubMed  Google Scholar 

  11. Delgado-García S, Martínez-Escoriza J-C, Alba A, Martín-Bayón T-A, Ballester-Galiana H, Peiró G, et al. Presence of human papillomavirus DNA in breast cancer: a Spanish case–control study. BMC Cancer. 2017;17:320. https://doi.org/10.1186/s12885-017-3308-3.

    Article  Google Scholar 

  12. 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. 1990;87:463–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yasmeen A, Bismar TA, Dekhil H, Ricciardi R, Kassab A, Gambacorti-Passerini C, et al. ErbB-2 receptor cooperates with E6/E7 oncoproteins of HPV Type 16 in breast tumorigenesis. Cell Cycle. 2007;6(23):2939–43. https://doi.org/10.4161/cc.6.23.4949.

    Article  CAS  Google Scholar 

  14. 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(6):541–4. https://doi.org/10.1016/j.breast.2010.05.007.

    Article  Google Scholar 

  15. Joshi D, Case G. Are viruses associated with human breast cancer? Scrutinizing the molecular evidence. Breast Cancer Res Treat. 2012;135:1–15. https://doi.org/10.1007/s10549-011-1921-4.

    Article  Google Scholar 

  16. Simoes PW, Medeiros LR, Pires PDS, Edelweiss MI, Rosa DD, Silva FR, et al. Prevalence of human papillomavirus in breast cancer a systematic review. Int J Gynecol Cancer. 2012;22:343–7. https://doi.org/10.1097/IGC.0b013e31823c712e.

    Article  Google Scholar 

  17. de Villiers E-M, Sandstrom RE, Hausen H, Buck CE. Presence of papillomavirus sequences in condylomatous lesions of the mamillae and in invasive carcinoma of the breast. Breast Cancer Res. 2005;7:R1–11. https://doi.org/10.1186/bcr940.

    Article  Google Scholar 

  18. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn H-J, et al. Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol. 2011;22:1736–47. https://doi.org/10.1093/annonc/mdr304.

    Article  CAS  Google Scholar 

  19. Husnjak K, Grce M, Magdic L, Pavelic K. Comparison of five different polymerase chain reaction methods for detection of human papillomavirus in cervical cell specimens. J Virol Methods 2000;88:125–134.

    Article  CAS  PubMed  Google Scholar 

  20. Fernandes A, Bianchi G, Feltri AP, Pérez M, Correnti M. Presence of human papillomavirus in breast cancer and its association with prognostic factors. eCancer. 2015;9:548. https://doi.org/10.3332/ecancer.2015.548.

    Article  Google Scholar 

  21. Corbex M, Bouzbid S, Traverse-Glehen A, Aouras H, McKay-Chopin 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(12):e114559. https://doi.org/10.1371/journal.pone.0114559.

    Article  Google Scholar 

  22. Elamrani A, Ennaji MM, Benhessou M, Attaleb M, El Mzibri M, Corbex M. Detection of human papillomavirus dna in breast cancer in moroccan woman. Ann Oncol. 2013;24(3):45. https://doi.org/10.1093/annonc/mdt086.12.

    Google Scholar 

  23. El-shinawi M, Mohamed HT, Abdel-Fattah HH, Ibrahim SAA, El-Halawany MS, Nouh MA, et al. Inflammatory and non-inflammatory breast cancer: a potential role for detection of multiple viral DNAs in disease progression. Ann Surg Oncol. 2015. https://doi.org/10.1245/s10434-015-4888-2.

    Google Scholar 

  24. 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;29:48–55. https://doi.org/10.1007/s12032-010-9812-9.

    Article  Google Scholar 

  25. de León DC, Montiel DP, Nemcova J, Mykyskova I, Turcios E, Villavicencio V, et al. Human Papillomavirus (HPV) in breast tumors: prevalence in a group of Mexican patients. BMC Cancer. 2009;9:26. https://doi.org/10.1186/1471-2407-9-26.

    Article  Google Scholar 

  26. Islam S, Dasgupta H, Roychowdhury A, Bhattacharya R, Mukherjee N, Roy A, 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. https://doi.org/10.1371/journal.pone.0172760.

    Article  Google Scholar 

  27. 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. 2007;7:33–6.

    Article  Google Scholar 

  28. Gumus M, Yumuk PF, 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;25:515–21.

    CAS  PubMed  Google Scholar 

  29. Akil N, Yasmeen A, Kassab A, Ghabreau L, Darmel A, 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 Clinical Studies. Br J Cancer. 2008;99:404–7. https://doi.org/10.1038/sj.bjc.6604503.

    Article  CAS  Google Scholar 

  30. Correnti M, Medina F, Eugenia M, Rennola A, Ávila M, Fernándes A. Gynecologic oncology human papillomavirus (HPV) type distribution in cervical carcinoma, low-grade, and high-grade squamous intraepithelial lesions in Venezuelan women. Gynecol Oncol. 2011;121(3):527–31. https://doi.org/10.1016/j.ygyno.2011.02.003.

    Article  Google Scholar 

  31. Boumba LMA, Hilali L, Mouallif M, Moukassa D, Ennaji MM. Specific genotypes of human papillomavirus in 125 high-grade squamous lesions and invasive cervical cancer cases from Congolese women. BMC Public Health. 2014;14:1320. https://doi.org/10.1186/1471-2458-14-1320.

    Article  Google Scholar 

  32. Hamidi-Fard M, Fattahi-Abdizadeh M, Makvandi M, Ranjbari N, Mansoori E, Samarbaf-Zadeh A. Detection and Genotyping of Human Papillomavirus in Cervical Tissue Samples in Ahvaz, Southwest Iran. Jundishapur J Microbiol. 2013;6(7):e4569. https://doi.org/10.5812/jjm.4569.

    Google Scholar 

  33. Omire A, Budambula N, Ochieng W, Baliach C, Keros D, Langat H, et al. Assessment of risk predisposition to human papilloma virus through cervical infections screening of women attending an outpatient health facility in Nairobi, Kenya. J Biol Agric Healthcare. 2014;4(22):28–36.

    Google Scholar 

  34. Herrera-Goepfert R, Vela-Chávez T, Carrillo-García A, Lizano-Soberón M, Amador-Molina A, Oñate-Ocaña LF, et al. High-risk human papillomavirus (HPV) DNA sequences in metaplastic breast carcinomas of Mexican women. BMC Cancer. 2013;13:445. https://doi.org/10.1186/1471-2407-13-445.

    Article  Google Scholar 

  35. 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(5):e97787. https://doi.org/10.1371/journal.pone.0097787.

    Article  Google Scholar 

  36. Kroupis C, Markou A, Vourlidis N, Dionyssiou-Asteriou A, Lianidou ES. Presence of high-risk human papillomavirus sequences in breast cancer tissues and association with histopathological characteristics. Clin Biochem. 2006;39:727–31. https://doi.org/10.1016/j.clinbiochem.2006.03.005.

    Article  CAS  Google Scholar 

  37. Lawson JS, Kan C, Iacopetta BJ, Whitaker NJ. Are some breast cancers sexually transmitted? Br J Cancer. 2006;95:1708. https://doi.org/10.1038/sj.bjc.6603502.

    Article  CAS  Google Scholar 

  38. Pike MC, Spicer DV, Dahmoush L, Press MF. Estrogens, progestogens, normal breast cell proliferation, and breast cancer risk. Epidemiol Rev. 1993;15(1):17–35.

    Article  CAS  PubMed  Google Scholar 

  39. Brake T, Lambert PF. Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc Natl Acad Sci. 2005;102:2490–5. https://doi.org/10.1073/pnas.0409883102.

    Article  CAS  Google Scholar 

  40. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, Stanley MA. The biology and life-cycle of human papillomaviruses. Vaccine. 2012;30S(5):F55–70. https://doi.org/10.1016/j.vaccine.2012.06.083.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Biology and Medical Research Unit in CNESTEN and the King Faisal Hospital and Kigali Teaching Hospital staff for their helpful collaboration.

Author information

Author notes

  1. Youssef Bakri and Mohammed El Mzibri contributed equally.

Authors and Affiliations

  1. Biology and Medical Research Unit, Centre National de l’Energie, des Sciences et des Techniques Nucléaires (CNESTEN), Rabat, Morocco

    Thierry Habyarimana, Mohammed Attaleb & Mohammed El Mzibri

  2. Biology of Human Pathologies Laboratory (BioPatH), Faculty of Science and Human Pathologies Center (GenoPatH), Mohammed V University (FSR - Mohammed V University), Rabat, Morocco

    Thierry Habyarimana & Youssef Bakri

  3. Biomedical Services Department, Rwanda Biomedical Center (RBC-BIOS), KN 4 Ave, Kigali, Rwanda

    Thierry Habyarimana & Jean Baptiste Mazarati

Authors
  1. Thierry Habyarimana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammed Attaleb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean Baptiste Mazarati
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Youssef Bakri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammed El Mzibri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thierry Habyarimana.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Habyarimana, T., Attaleb, M., Mazarati, J.B. et al. Detection of human papillomavirus DNA in tumors from Rwandese breast cancer patients. Breast Cancer 25, 127–133 (2018). https://doi.org/10.1007/s12282-018-0831-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12282-018-0831-2

Keywords

Search

Navigation