Skip to main content
Download PDF

No detection of EBV, BKV and JCV in breast cancer tissue samples in Iran

BMC Research Notes volume 12, Article number: 171 (2019) Cite this article

Abstract

Objective

The most common cancer amongst women is breast cancer. Reports on the role of EBV, BKV, and JCV in the development of breast cancer are controversial. Hence, the aim of this study was to determine the frequency of EBV, BKV, and JCV in malignant breast tumors in comparison with benign ones.

Results

A total of 300 breast biopsy tissues were included, of which 150 were malignant and 150 benign. After deparaffinization, tissues were subjected to DNA extraction. β-globin gene was amplified by PCR to evaluate the quality of extracted DNA. In house PCRs assay was performed to detect EBV, JCV, and BKV genome fragment. The mean age of malignant and benign groups was 45.0 ± 9.4 and 35.2 ± 12.1 years old. Out of 150 malignant samples, 146 were ductal, two lobular and two samples both invasive ductal and lobular carcinoma. In the benign group, 96, 52 and two samples were fibroadenoma, fibrocystic, and adenosis types, respectively. Genomic DNA fragment of EBV, BKV, and JCV was not found in any of the malignant and benign breast tissues.

Conclusion

According to our finding, there is the possibility that EBV, BKV, and JCV are not involved in breast cancer pathogenesis.

Introduction

According to a recent report, there are 17.5 million cancer cases and 8.7 million related deaths worldwide [1]. Among cancers, breast cancer is the most common cancer with around 2.4 million cases in 2015 [1]. In Iran, there are 4000 related deaths and 7000 new cases annually and with the incidence rate is 24 per 100,000 people, as the most common type of cancer amongst Iranian women [2].

Environmental, hereditary and genetic background are considered as the most important factors involved in breast cancer development/progression. Among environmental factors, viral infections appear to be associated with about 15–20% of all cancers [3]. Viruses including Hepatitis B virus (HBV), Epstein Barr virus (EBV), Human polyomavirus (HPV) as well as some polyomaviruses such as Merkel cell polyomavirus (MCPyV), BK virus (BKV), and John Cunningham virus (JCV) have been associated with human cancers [4, 5].

EBV role in the pathogenesis of several malignancies, including Burkittlymphoma, nasopharyngeal carcinoma, and gastric cancer has been verified, but its role on breast carcinoma development remains to be determined [3, 6]. EBV resides in B lymphocyte cells with access to breast tissues that leads to infected breast epithelial cells [7]. Hence, there is a possibility that EBV might increase the risk of breast cancer [6]. EBV proteins, expressed in the latent/productive cycle might have an important role in cell transformation. Matrix metallopeptidase 9 induced by BZLF1 forms complexes with P53 and P56, which does not allow infected cells to become apoptosis. Moreover, BRL1 induces E2F, by entering the infected cells to S-phase and proliferation [8]. In addition, late membrane protein1 (LMP1) and 2 mimic cellular receptors continuously active signaling pathways that induce proliferation and survival of the infected cells. Furthermore, miRNAs encoded by EBV have an important role in immune evasion and cell survival [9].

BKV and JCV are members of Polyomaviruses family, and human is the sole host of BKV and JCV [10]. Primary infection by JCV and BKV are predominantly asymptomatic and the viruses persist in kidney and B lymphocytes [11]. Since 1953, polyomaviruses have been considered as etiologic agents in cancer, when Gross et al. discovered murine polyomavirus. JCV and BKV contain a double strand DNA (dsDNA) genome, which encodes two oncoproteins called large T antigen (T-Ag) and small t antigen (t-Ag) that are involved in cell transformation [12]. BKV Large T-Ag binds to the tumor suppressor proteins including retinoblastoma-associated protein (RB) and p53 leads to cycle progression as well as apoptosis inhibition [13]. JCV T-Ag activates ataxia-telangiectasia mutated (ATM)/ATM-and Rad3-Related (ATR) mediated G2 checkpoint pathways, causing G2 cell cycle arrest. Moreover, T-Ag can cause DNA damage by inhibiting homologous recombination directed DNA repair through its interaction with IRS1; hence, generating genetic instability in JCV containing cells [14, 15]. In addition, these viruses induce chromosomal aberrations in cells and by a ‘hit and run’ mechanism recruiting the neighboring cells and distant cell proliferation. They also establish latent infection throughout life and their T-Ag is detected in different types of human cancers [4, 10, 16].

Cancer is the third cause of mortality in Iran [17] and between different type of cancer, breast cancer was the second most common cause of death in 2015 [1]. Moreover, the most common types of primary breast cancer in the Iranian population are invasive ductal carcinoma and invasive lobular carcinoma with frequencies of 77.8% and 5.2% [18]. To the best of our knowledge, few studies have investigated the role of EBV, JCV and BKV in breast carcinomas in our region; hence, we conducted this study in the city of Shiraz, Iran.

Main text

Subjects and methods

A total of 300 breast tissue biopsies including 150 malignant and 150 benign tissue specimens were collected from Faghihi Hospital and Motahari clinic affiliated to Shiraz University of Medical Sciences. All cases had surgery from January 2008 to December 2015. Tissues were selected according to the pathology reports and had been verified by an expert pathologist. This study was approved by the local Ethics Committee of Shiraz University of Medical Sciences (Approval No. IR.SUMS.REC.1394.S372).

DNA extraction and qualification

Deparaffinization and DNA extraction were done as previously described [19, 20]. Polymerase chain reaction (PCR) with consensus primers PCO3/PCO4 (Table 1) was performed to amplify β-globin gene fragments to confirm the quality of extracted DNA. PCR for amplifying β-globin gene was performed as previously described [20]. A total of 321 samples were selected for assessment, of which 21 samples were excluded based on the ß-globin gene negative PCR result.

Table 1 The Sequences and other characteristics of primers used in this study
Full size table

EBV genome detection

To investigate the presence of the EBV genome fragment, AlleleID 7 software was used. The designing primers, specific for the BHRF1 region of the virus are shown in Table 1. EBV genome amplification was done on samples that were positive for the β-globin gene. PCR mix reaction components were 2×PCR master mix red (Ampliqon, Denmark) and 0.4 µM of each primer in 25 µl final volume. PCR tests for BHRF1 coding region of EBV was performed as follow: 10 min initial denaturation at 95 °C, 45 cycles of denaturation at 95 °C for 45 s, annealing at 57.6 °C for 45 s, extension at 72 °C for 45 s and final extension at 72 °C for 10 min. PCR products were then loaded into 2% agarose gel and visualized under UV light. The DNA extracted from the B-95 cell line (Institute pasture, Tehran, Iran) was used as a positive control during each run.

JCV genome detection

Also, positive breast tissue samples for the β-globin gene underwent PCR to detect JCV. Specific primers targeting JCV Large T antigen were selected from previous studies (Table 1) [21]. PCR was performed in a mix containing 1 mM MgCl2, 200 μM dNTPs, 1U Taq DNA polymerase (CinnaGene, Tehran, Iran) and 1 μM each specific primer in a total volume of 25 μL (Table 1). PCR program was as follow: 10 min initial denaturation at 95 °C, 50 cycles of denaturation at 95 °C for 1 min, annealing at 48 °C for 1 min, extension at 72 °C for 2 min, and final extension at 72 °C for 8 min. Then PCR products were loaded into 2% agarose gel and visualized under UV light. A positive control for JCV was provided by Keyvan Virology Laboratory (Tehran, Iran).

BKV genome detection

We also performed PCR to detect BKV in breast tissue samples as previously describe [21].

Results

Demographic and pathological result

Out of 150 malignant samples, 146 (97.3%) ductal, two (1.3%) lobular and the other two (1.3%) were both invasive ductal and lobular carcinoma. The mean age of participants in malignant and benign groups was 45.0 ± 9.4 SD and 35.2 ± 12.1 SD. Out of 150 malignant samples 35 (23.3%), 67(44.7%) and 48 (32%) were at stage I, II and III, respectively based on the American Joint Committee on Cancer system. In the case of benign samples, 96 (64%) were fibroadenoma, 52 (34.7%) were fibrocystic and 2 (1.3%) were adenosis type.

PCR for detection of EBV, JCV, and BKV

In our study, none of the cancerous and benign breast tumor tissues were positive for the presence of EBV, JCV and BKV DNA fragment as shown in Fig. 1.

Fig. 1
figure 1

Photographs of gel electrophoresis. M: 100 bp DNA size marker; lanes 1: positive control; lanes 2: sample; lanes 3: Negative control. a PCR analysis of DNA samples extracted from breast tissue using β- globin primers. b PCR analysis of DNA samples extracted from breast tissue using EBV common primers. c PCR analysis of DNA samples extracted from breast tissue using type-specific primers for JCV. d PCR analysis of DNA samples extracted from colorectal tissue using type-specific primers for BKV

Full size image

Discussion

Breast cancer is the main type of cancer amongst women [1]. Certain risk factors including age, early menstrual period, late or no pregnancy, menopause after age 55, not being physically active, taking oral contraceptives, family history of breast cancer, alcohol consumption, and smoking, have been proposed as risk factors for breast cancer development/progression [22].

The result of our study showed that none of the cancerous and benign samples were positive for EBV. In line with this finding, Perrigoue et al. found that all of the 45 tumor biopsies samples were negative for EBV DNA fragment [23]. Also, in Iran, Kadivar et al. showed that all cancerous and noncancerous tissue samples were negative for EBV DNA and protein [24]. On the other hand, Louise et al. reported an association between EBV and breast cancer [25]. Moreover, Bonnet et al. showed a higher frequency of EBV in cancerous tissue in comparison with healthy controls [26]. In addition, Mazouni et al. revealed that the frequency of EBV in breast cancer tissue was higher in more aggressive phenotype tumors [27]. Also, Zekri et al. showed the association of EBV with breast cancer [28]. Furthermore, in a study by Antonsson et al. 10% (5/54) of breast tumor samples were positive for EBV genome [29]. In Iran, in a case–control study, EBV was detected in breast cancer tissues, while all the control samples were negative for EBV [30].

Finally, the two meta-analysis by Huo et al. and Amarante et al. showed a significant association between EBV and breast cancer [31, 32]. A reason to investigate the association between EBV and breast cancer is that EBV infection confers resistance to an anticancer chemotherapy drug [8].

Although some reports showed the presence of EBV in breast cancer, others reported the absence of EBV genome/protein in breast cancer tissue. This difference might be due to limitation of the detection methods. As evidence, low levels of EBV genome was found in breast tumors by TaqMan real-time PCR while negative result was obtained in studies with less sensitive methods [33]. Also ‘hit and run’ mechanism was proposed as EBV oncogenesis; hence, the viral genome might be lost during malignant cell division [7].

In the case of JCV, none of the 150 malignant and 150 benign samples were positive for the JCV genome. In agreement with our results, Antonsson et al. reported that none of the 54 breast tumor samples were positive for JCV [29]. On the other hand, Hachana et al. reported that 23% (28/123) of breast cancer tissues were infected with JCV [34]. In addition, Moore et al. tested the milk from women with and without breast cancer history and found higher virus particles in the milk of women with familial history of breast cancer [35].

In our study, none of the malignant and benign breast tissues were positive for BKV genome fragment. In line with our result, Hachana et al. reported that BKV was not detected in breast carcinoma tissues of Tunisian patients [34]. Antonsson et al. also showed that none of the 54 breast tumor samples were positive for BKV [29]. Generally, low JCV and BKV DNA detection in tumors can be explained as the transient effect of JCV in cellular transformation, which is called “hit and run’’ transformation mechanism [36]. Different laboratory methods and/or sample size, population, geographic, and differences in the detection limit of the methods inevitably might explain the controversy. In conclusion, the results of our study revealed that the DNA fragment of EBV, JCV, and BKV was not detected in any of the malignant and benign breast samples. Therefore, it can be said that there is no association between EBV, JCV, and BKV infection and breast cancer. To identify the role of these viruses in breast cancer, more investigations with larger sample sizes and more sensitive methods are recommended.

Limitations

It can be noted that the limitations of our study were working on formalin-fixed paraffin-embedded tissue specimens as well as using conventional PCR assay, which can be resolved in similar future studies, by performing real-time PCR on fresh biopsy specimens.

Abbreviations

HBV:

Hepatitis B virus

HCV:

Hepatitis C virus

EBV:

Epstein Barr virus

HPV:

human papillomavirus

MCPyV:

Merkel cell polyomavirus

BKV:

Thea Brennan-Krohn virus

JCV:

John Cunningham virus

dsDNA:

double strand DNA

LMP1:

late membrane protein1

AIDS:

acquired immune deficiency syndrome

RB:

retinoblastoma-associated protein

ATM:

ataxia-telangiectasia mutated

PCR:

polymerase chain reaction

References

  1. Global Burden of Disease Cancer C, Fitzmaurice C, Allen C, Barber RM, Barregard L, Bhutta ZA, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 32 cancer groups, 1990 to 2015: a systematic analysis for the global burden of disease study. JAMA Oncol. 2017;3(4):524–48. https://doi.org/10.1001/jamaoncol.2016.5688.

    Article  Google Scholar 

  2. Mahdavifar N, Pakzad R, Ghoncheh M, Pakzad I, Moudi A, Salehiniya H. Spatial analysis of breast cancer incidence in Iran. Asian Pac J Cancer Prev. 2016;17(S3):59–64.

    Article  Google Scholar 

  3. Wong M, Pagano JS, Schiller JT, Tevethia SS, Raab-Traub N, Gruber J. New associations of human papillomavirus, Simian virus 40, and Epstein-Barr virus with human cancer. J Natl Cancer Inst. 2002;94(24):1832–6.

    Article  CAS  Google Scholar 

  4. Alibek K, Kakpenova A, Mussabekova A, Sypabekova M, Karatayeva N. Role of viruses in the development of breast cancer. Infect Agent Cancer. 2013;8:32. https://doi.org/10.1186/1750-9378-8-32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sarvari J, Mojtahedi Z, Kuramitsu Y, Fattahi MR, Ghaderi A, Nakamura K, et al. Comparative proteomics of Sera from HCC patients with different origins. Hepat Mon. 2014;14(1):e13103. https://doi.org/10.5812/hepatmon.13103.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Richardson AK, Currie MJ, Robinson BA, Morrin H, Phung Y, Pearson JF, et al. Cytomegalovirus and Epstein-Barr virus in breast cancer. PLoS ONE. 2015;10(2):e0118989. https://doi.org/10.1371/journal.pone.0118989.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Magrath I, Bhatia K. Breast cancer: a new Epstein-Barr virus-associated disease? J Natl Cancer Inst. 1999;91(16):1349–50.

    Article  CAS  Google Scholar 

  8. Arbach H, Viglasky V, Lefeu F, Guinebretiere JM, Ramirez V, Bride N, et al. Epstein-Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxel (Taxol). J Virol. 2006;80(2):845–53. https://doi.org/10.1128/JVI.80.2.845-853.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zuo L, Yue W, Du S, Xin S, Zhang J, Liu L, et al. An update: Epstein-Barr virus and immune evasion via microRNA regulation. Virol Sin. 2017;32(3):175–87. https://doi.org/10.1007/s12250-017-3996-5.

    Article  CAS  PubMed  Google Scholar 

  10. Assetta B, Atwood WJ. The biology of JC polyomavirus. Biol Chem. 2017;398(8):839–55. https://doi.org/10.1515/hsz-2016-0345.

    Article  CAS  PubMed  Google Scholar 

  11. Dalianis T, Hirsch HH. Human polyomaviruses in disease and cancer. Virology. 2013;437(2):63–72. https://doi.org/10.1016/j.virol.2012.12.015.

    Article  CAS  PubMed  Google Scholar 

  12. Polz D, Stec A, Polz-Dacewicz M. BK-virus (BKV)–structure, epidemiology and pathogenesis. J Pre-Clin Clin Res. 2013;7(2):90–2.

    Google Scholar 

  13. Gossai A, Waterboer T, Nelson HH, Doherty JA, Michel A, Willhauck-Fleckenstein M, et al. Prospective study of human polyomaviruses and risk of cutaneous squamous cell carcinoma in the United States. Cancer Epidemiol Biomarkers Prev. 2016;25(5):736–44. https://doi.org/10.1158/1055-9965.EPI-15-1111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Coelho TR, Almeida L, Lazo PA. JC virus in the pathogenesis of colorectal cancer, an etiological agent or another component in a multistep process? Virol J. 2010;7:42. https://doi.org/10.1186/1743-422X-7-42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nali LH, Centrone Cde C, Urbano PR, Penalva-de-Oliveira AC, Vidal JE, Miranda EP, et al. High prevalence of the simultaneous excretion of polyomaviruses JC and BK in the urine of HIV-infected patients without neurological symptoms in Sao Paulo, Brazil. Rev Inst Med Trop Sao Paulo. 2012;54(4):201–5.

    Article  Google Scholar 

  16. Tognon M, Corallini A, Martini F, Negrini M, Barbanti-Brodano G. Oncogenic transformation by BK virus and association with human tumors. Oncogene. 2003;22(33):5192–200. https://doi.org/10.1038/sj.onc.1206550.

    Article  CAS  PubMed  Google Scholar 

  17. Bakhtiarizadeh S, Hosseini SY, Yaghobi R, Safaei A, Sarvari J. Almost complete lack of human cytomegalovirus and human papillomaviruses genome in benign and malignant breast lesions in Shiraz, Southwest of Iran. Asian Pac J Cancer Prev. 2017;9(12):3319–24.

    Google Scholar 

  18. Jazayeri SB, Saadat S, Ramezani R, Kaviani A. Incidence of primary breast cancer in Iran: ten-year national cancer registry data report. Cancer Epidemiol. 2015;39(4):519–27. https://doi.org/10.1016/j.canep.2015.04.016.

    Article  PubMed  Google Scholar 

  19. Mahmoudvand S, Zamani K, Safaei A, Khashei R, Motamedifar M, Azizi Z, et al. No detection of Streptococcus gallolyticus and Helicobacter pylori in colorectal cancer tissue samples in Shiraz, Iran. Iran J Cancer Prev. 2017;10(1):e6337. https://doi.org/10.17795/ijcp-6337.

    Article  Google Scholar 

  20. Mahmoudvand S, Safaei A, Erfani N, Sarvari J. Presence of human papillomavirus DNA in colorectal cancer tissues in Shiraz, Southwest Iran. Asian Pac J Cancer Prev. 2015;16(17):7883–7.

    Article  Google Scholar 

  21. Sarvari J, Mahmoudvand S, Pirbonyeh N, Safaei A, Hosseini SY. The very low frequency of Epstein-Barr, JC and BK viruses DNA in colorectal cancer tissues in Shiraz, Southwest Iran. Polish J Microbiol. 2018;67:73–9.

    Article  Google Scholar 

  22. Ochsendorf F. Sexually transmitted infections: impact on male fertility. Andrologia. 2008;40(2):72–5.

    Article  CAS  Google Scholar 

  23. Perrigoue JG, den Boon JA, Friedl A, Newton MA, Ahlquist P, Sugden B. Lack of association between EBV and breast carcinoma. Cancer Epidemiol Biomarkers Prev. 2005;14(4):809–14. https://doi.org/10.1158/1055-9965.EPI-04-0763.

    Article  CAS  PubMed  Google Scholar 

  24. Kadivar M, Monabati A, Joulaee A, Hosseini N. Epstein-Barr virus and breast cancer: lack of evidence for an association in Iranian women. Pathol Oncol Res. 2011;17(3):489–92. https://doi.org/10.1007/s12253-010-9325-z.

    Article  PubMed  Google Scholar 

  25. Labrecque LG, Barnes DM, Fentiman IS, Griffin BE. Epstein-Barr virus in epithelial cell tumors: a breast cancer study. Cancer Res. 1995;55(1):39–45.

    CAS  PubMed  Google Scholar 

  26. Bonnet M, Guinebretiere JM, Kremmer E, Grunewald V, Benhamou E, Contesso G, et al. Detection of Epstein-Barr virus in invasive breast cancers. J Natl Cancer Inst. 1999;91(16):1376–81.

    Article  CAS  Google Scholar 

  27. Mazouni C, Fina F, Romain S, Ouafik L, Bonnier P, Brandone JM, et al. Epstein-Barr virus as a marker of biological aggressiveness in breast cancer. Br J Cancer. 2011;104(2):332–7. https://doi.org/10.1038/sj.bjc.6606048.

    Article  CAS  PubMed  Google Scholar 

  28. Zekri AR, Bahnassy AA, Mohamed WS, El-Kassem FA, El-Khalidi SJ, Hafez MM, et al. 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. https://doi.org/10.1016/j.jnci.2012.06.001.

    Article  PubMed  Google Scholar 

  29. Antonsson A, Bialasiewicz S, Rockett RJ, Jacob K, Bennett IC, Sloots TP. Exploring the prevalence of ten polyomaviruses and two herpes viruses in breast cancer. PLoS ONE. 2012;7(8):e39842. https://doi.org/10.1371/journal.pone.0039842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Reza MA, Reza MH, Mahdiyeh L, Mehdi F, Hamid ZN. Evaluation frequency of Merkel cell polyoma, Epstein-Barr and mouse mammary tumor viruses in patients with breast cancer in Kerman, Southeast of Iran. Asian Pac J Cancer Prev. 2015;16(16):7351–7.

    Article  Google Scholar 

  31. 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  PubMed  PubMed Central  Google Scholar 

  32. Amarante MK, Watanabe MA. The possible involvement of virus in breast cancer. J Cancer Res Clin Oncol. 2009;135(3):329–37. https://doi.org/10.1007/s00432-008-0511-2.

    Article  PubMed  Google Scholar 

  33. Perkins RS, Sahm K, Marando C, Dickson-Witmer D, Pahnke GR, Mitchell M, et al. Analysis of Epstein-Barr virus reservoirs in paired blood and breast cancer primary biopsy specimens by real time PCR. Breast Cancer Res. 2006;8(6):R70. https://doi.org/10.1186/bcr1627.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Hachana M, Amara K, Ziadi S, Gacem RB, Korbi S, Trimeche M. Investigation of human JC and BK polyomaviruses in breast carcinomas. Breast Cancer Res Treat. 2012;133(3):969–77. https://doi.org/10.1007/s10549-011-1876-5.

    Article  CAS  PubMed  Google Scholar 

  35. Moore DH, Charney J, Kramarsky B, Lasfargues EY, Sarkar NH, Brennan MJ, et al. Search for a human breast cancer virus. Nature. 1971;229(5287):611–4.

    Article  CAS  Google Scholar 

  36. Loutfy SA, Moneer MM, Salem SE, El-Moniem Abada EA, El-Moniem Ahmed EA, Ibrahim LH, et al. Polyomavirus infections and its clinical relevance in cancer patients: a Prospective Study. J Infect Public Health. 2017;10(1):22–30. https://doi.org/10.1016/j.jiph.2016.01.008.

    Article  PubMed  Google Scholar 

Download references

Authors’ contributions

RD and JS: conceived the study. SM, AA, RA, SB: participated in the design of the study and performed the statistical analysis. AS, NJ: Practical work. NJ: obtained ethical clearance and permission for study. AS, JS, RD: Drafting the article or revisiting it critically for important intellectual content. NJ and RD were project leaders and primary investigators of the study. All authors read and approved the final manuscript.

Acknowledgements

The present study was extracted from the thesis written by Abootaleb Alidadi, Rasool Alizadeh and Sara Mir-Rashidi. The authors wish to thank Mr. H. Argasi at the Research Consultation Center (RCC) of Shiraz University of Medical Sciences for his invaluable assistance in editing this manuscript.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Consent for publication

Not applicable.

Ethics approval and consent to participate

This study was in accordance with the declaration of Helsinki and an ethical permission was sought from the institutional Ethics Committee of Shiraz University of Medical Sciences (Approval No. IR.SUMS.REC.1394.S372). However, because we only used paraffin-embedded tissue of clinical specimens that already were produced, the local ethics committee waived the need for informed consent.

Funding support

This study was supported by Shiraz University of Medical Sciences, Shiraz, Iran with Grant Nos. 94-9816, 94-9817 and 96-16352. This funding source had no role in the design of this study and will not have any role during its execution, analyses, interpretation of the data, or decision to submit results.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Author information

Authors and Affiliations

  1. Department of Bacteriology & Virology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

    Razieh Dowran, Negar Joharinia, Sahar Bakhtiyarizadeh, Abootaleb Alidadi Soleimani, Rasool Alizadeh, Sara Mir-Shiri & Jamal Sarvari

  2. Department of Pathology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

    Akbar Safaei

  3. Gastroenterohepatology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

    Jamal Sarvari

Authors
  1. Razieh Dowran
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Negar Joharinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akbar Safaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sahar Bakhtiyarizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abootaleb Alidadi Soleimani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rasool Alizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sara Mir-Shiri
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jamal Sarvari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jamal Sarvari.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dowran, R., Joharinia, N., Safaei, A. et al. No detection of EBV, BKV and JCV in breast cancer tissue samples in Iran. BMC Res Notes 12, 171 (2019). https://doi.org/10.1186/s13104-019-4178-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13104-019-4178-3

Keywords

BMC Research Notes

ISSN: 1756-0500

Contact us