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Published in: Tumor Biology 1/2013

01-02-2013 | Research Article

Association of human herpes, papilloma and polyoma virus families with bladder cancer

Authors: Georgios I. Panagiotakis, Danae Papadogianni, Maria N. Chatziioannou, Ismini Lasithiotaki, Dimitrios Delakas, Demetrios A. Spandidos

Published in: Tumor Biology | Issue 1/2013

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Abstract

The aim of the present study was to assess the possible etiologic role of human papillomavirus (HPV), human herpes virus (HHV) and the human polyoma virus families (BKV and JCV) in the tumourigenesis of bladder cancer. Thirty biopsy specimens from patients with different grades and stages of bladder cancer, who underwent transurethral bladder cancer resection, and 30 normal bladder mucosa specimens were analysed using polymerase chain reaction (PCR) for the detection of the above three virus family members. The presence of HPV was determined in all specimens with nested PCR and real-time quantitative PCR. All cancerous specimens, including the control group, were found to be negative both by PCR and real-time qPCR for the presence of HPV DNA, whilst all samples examined by PCR tested negative for the presence of HSV-1,2 Varicella zoster virus and HSV-7 DNA. Cytomegalovirus, HHV-6 and HHV-8 exhibited similar incidence in sample positivity in both cancerous and healthy tissues. EBV showed a higher prevalence in bladder cancer specimens compared to healthy tissue (p = 0.048), whilst BKV and JCV were detected only in tumour samples. The presence of EBV in a significant proportion of bladder tumours indicates the etiological role of this virus in cancer tumourigenesis.
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Literature
1.
go back to reference Pashos CL, Botteman MF, Laskin BL, Redaelli A. Bladder cancer: epidemiology, diagnosis, and management. Cancer Pract. 2002;10:311–22.PubMedCrossRef Pashos CL, Botteman MF, Laskin BL, Redaelli A. Bladder cancer: epidemiology, diagnosis, and management. Cancer Pract. 2002;10:311–22.PubMedCrossRef
3.
go back to reference Mammas IN, Sourvinos G, Michael C, Spandidos DA. Human papilloma virus in hyperplastic tonsillar and adenoid tissues in children. Pediatr Infect Dis J. 2006;25:1158–62.PubMedCrossRef Mammas IN, Sourvinos G, Michael C, Spandidos DA. Human papilloma virus in hyperplastic tonsillar and adenoid tissues in children. Pediatr Infect Dis J. 2006;25:1158–62.PubMedCrossRef
4.
go back to reference Zderic SA, Carpiniello VL, Malloy TR, Rando RF. Urological applications of human papillomavirus typing using deoxyribonucleic acid probes for the diagnosis and treatment of genital condyloma. J Urol. 1989;141:63–5.PubMed Zderic SA, Carpiniello VL, Malloy TR, Rando RF. Urological applications of human papillomavirus typing using deoxyribonucleic acid probes for the diagnosis and treatment of genital condyloma. J Urol. 1989;141:63–5.PubMed
5.
go back to reference Libby JM, Frankel JM, Scardino PT. Condyloma acuminatum of the bladder and associated urothelial malignancy. J Urol. 1985;134:134–6.PubMed Libby JM, Frankel JM, Scardino PT. Condyloma acuminatum of the bladder and associated urothelial malignancy. J Urol. 1985;134:134–6.PubMed
6.
go back to reference Mevorach RA, Cos LR, di Sant’Agnese PA, Stoler M. Human papillomavirus type 6 in grade I transitional cell carcinoma of the urethra. J Urol. 1990;143:126–8.PubMed Mevorach RA, Cos LR, di Sant’Agnese PA, Stoler M. Human papillomavirus type 6 in grade I transitional cell carcinoma of the urethra. J Urol. 1990;143:126–8.PubMed
7.
go back to reference Di Paolo JA, Woodworth CD, Popescu NC, Koval DL, Lopez JV, Doniger J. HSV-2-induced tumorigenicity in HPV-16 immortalized human genital keratinocytes. Virology. 1990;177:777–9.CrossRef Di Paolo JA, Woodworth CD, Popescu NC, Koval DL, Lopez JV, Doniger J. HSV-2-induced tumorigenicity in HPV-16 immortalized human genital keratinocytes. Virology. 1990;177:777–9.CrossRef
8.
go back to reference Hildesheim A, Mann V, Brinton LA, Szklo M, Reeves WC, Rawls WE. Herpes simplex virus type 2: a possible interaction with human papilloma virus types 16/18 in the development of invasive cervical cancer. Int J Cancer. 1991;49:335–40.PubMedCrossRef Hildesheim A, Mann V, Brinton LA, Szklo M, Reeves WC, Rawls WE. Herpes simplex virus type 2: a possible interaction with human papilloma virus types 16/18 in the development of invasive cervical cancer. Int J Cancer. 1991;49:335–40.PubMedCrossRef
9.
go back to reference Kjaer SK, De Villiers EM, Çaglayan H, Svare E, Haugaard BJ, Engholm G, et al. Human papillomavirus, herpes simplex virus and other potential risk factors for cervical cancer in a high-risk area (Greenland) and a low-risk area (Denmark)—a second look. Br J Cancer. 1993;67:830–7.PubMedCrossRef Kjaer SK, De Villiers EM, Çaglayan H, Svare E, Haugaard BJ, Engholm G, et al. Human papillomavirus, herpes simplex virus and other potential risk factors for cervical cancer in a high-risk area (Greenland) and a low-risk area (Denmark)—a second look. Br J Cancer. 1993;67:830–7.PubMedCrossRef
10.
go back to reference Schmauz R, Okong P, De Villiers E-M, Dennin R, Brade L, Lwanga SK, et al. Multiple infections in cases of cervical cancer from a high-incidence area in tropical Africa. Int J Cancer. 1989;43:805–9.PubMedCrossRef Schmauz R, Okong P, De Villiers E-M, Dennin R, Brade L, Lwanga SK, et al. Multiple infections in cases of cervical cancer from a high-incidence area in tropical Africa. Int J Cancer. 1989;43:805–9.PubMedCrossRef
11.
go back to reference Landers RJ, O’Leary JJ, Crowley M, Annis P, Burke L, O’Brien D, et al. Epstein–Barr virus in normal, premalignant lesions of the uterine cervix. J Clin Pathol. 1993;46:931–5.PubMedCrossRef Landers RJ, O’Leary JJ, Crowley M, Annis P, Burke L, O’Brien D, et al. Epstein–Barr virus in normal, premalignant lesions of the uterine cervix. J Clin Pathol. 1993;46:931–5.PubMedCrossRef
12.
go back to reference Wong KY, Colins RJ, Srivastava G, Pittaluga S, Cheung ANY, Wong LC. Epstein–Barr virus in carcinoma of the cervix. Intern J Gynec Pathol. 1993;12:224–7.CrossRef Wong KY, Colins RJ, Srivastava G, Pittaluga S, Cheung ANY, Wong LC. Epstein–Barr virus in carcinoma of the cervix. Intern J Gynec Pathol. 1993;12:224–7.CrossRef
13.
go back to reference Israele V, Shirley P, Sixbey JW. Excretion of the Epstein–Barr virus from the genital tract of men. J Infect Dis. 1991;163:1341–3.PubMedCrossRef Israele V, Shirley P, Sixbey JW. Excretion of the Epstein–Barr virus from the genital tract of men. J Infect Dis. 1991;163:1341–3.PubMedCrossRef
14.
go back to reference Hung SY, Tseng HH, Chung HM. Nephrogenic adenoma associated with cytomegalovirus infection of the ureter in a renal transplant patient: presentation as ureteral obstruction. Transpl Int. 2001;14:111–4.PubMedCrossRef Hung SY, Tseng HH, Chung HM. Nephrogenic adenoma associated with cytomegalovirus infection of the ureter in a renal transplant patient: presentation as ureteral obstruction. Transpl Int. 2001;14:111–4.PubMedCrossRef
15.
go back to reference Escudero AL, Luque RJ, Quintero A, Alvarez-Kindelan J, Requena M, Montironi R, et al. Association of human herpesvirus type 6 DNA with human bladder cancer. Cancer Lett. 2005;230:20–4.PubMedCrossRef Escudero AL, Luque RJ, Quintero A, Alvarez-Kindelan J, Requena M, Montironi R, et al. Association of human herpesvirus type 6 DNA with human bladder cancer. Cancer Lett. 2005;230:20–4.PubMedCrossRef
16.
go back to reference Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, et al. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA. 1996;93:14862–7. Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, et al. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA. 1996;93:14862–7.
17.
go back to reference Major EO. Human polyomavirus. In: Knipe D, Howley PM, editors. Fields virology, 4th edition, vol. 2 (edited by Lipincott). Philadelphia: Williams & Wilkins; 2001. p. 2175–96. Major EO. Human polyomavirus. In: Knipe D, Howley PM, editors. Fields virology, 4th edition, vol. 2 (edited by Lipincott). Philadelphia: Williams & Wilkins; 2001. p. 2175–96.
18.
go back to reference Weinreb DB, Desman GT, Amolat-Apiado MJM, Burstein DE, Jr Godbold JH, Johnson EM. Polyoma virus infection is a prominent risk factor for bladder carcinoma in immunocompetent individuals. Diagn Cytopathol. 2006;34:201–3.PubMedCrossRef Weinreb DB, Desman GT, Amolat-Apiado MJM, Burstein DE, Jr Godbold JH, Johnson EM. Polyoma virus infection is a prominent risk factor for bladder carcinoma in immunocompetent individuals. Diagn Cytopathol. 2006;34:201–3.PubMedCrossRef
19.
go back to reference De Roda Husman A-M, Walboomers JMM, van den Brule AJC, Meijer CJ, Snijders PJ. The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol. 1995;76:1057–62.CrossRef De Roda Husman A-M, Walboomers JMM, van den Brule AJC, Meijer CJ, Snijders PJ. The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol. 1995;76:1057–62.CrossRef
20.
go back to reference Neofytou E, Sourvinos G, Asmarianaki M, Spandidos DA, Makrigiannakis A. Prevalence of human herpes virus types 1–7 in the semen of men attending an infertility clinic and correlation with semen parameters. Fertil Steril. 2009;91:2487–94.PubMedCrossRef Neofytou E, Sourvinos G, Asmarianaki M, Spandidos DA, Makrigiannakis A. Prevalence of human herpes virus types 1–7 in the semen of men attending an infertility clinic and correlation with semen parameters. Fertil Steril. 2009;91:2487–94.PubMedCrossRef
21.
go back to reference Balis V, Sourvinos G, Soulitzis N, Giannikaki E, Sofras F, Spandidos DA. Prevalence of BK virus and human papillomavirus in human prostate cancer. Int J Biol Markers. 2007;22:245–51.PubMed Balis V, Sourvinos G, Soulitzis N, Giannikaki E, Sofras F, Spandidos DA. Prevalence of BK virus and human papillomavirus in human prostate cancer. Int J Biol Markers. 2007;22:245–51.PubMed
22.
go back to reference Dokianakis DN, Sourvinos G, Sakkas S, Athanasiadou E, Spandidos DA. Detection of HPV and ras gene mutations in cervical smears from female genital lesions. Oncol Rep. 1998;5:1195–8.PubMed Dokianakis DN, Sourvinos G, Sakkas S, Athanasiadou E, Spandidos DA. Detection of HPV and ras gene mutations in cervical smears from female genital lesions. Oncol Rep. 1998;5:1195–8.PubMed
23.
go back to reference Panagiotakis SH, Soufla G, Baritaki S, Sourvinos G, Passam A, Zagoreos I, et al. Concurrent CMV and EBV DNAemia is significantly correlated with a delay in the response to HAART in treatment-naive HIV type 1-positive patients. AIDS Res Hum Retrovir. 2007;23:10–8.PubMedCrossRef Panagiotakis SH, Soufla G, Baritaki S, Sourvinos G, Passam A, Zagoreos I, et al. Concurrent CMV and EBV DNAemia is significantly correlated with a delay in the response to HAART in treatment-naive HIV type 1-positive patients. AIDS Res Hum Retrovir. 2007;23:10–8.PubMedCrossRef
24.
go back to reference Baltogiannis D, Tasos A, Voutsinas G, Dauaher H, Chambilomatis P, Giannakopoulos X. Bladder cancer mortality in the Epirus district population (Greece). Int Urol Nephrol. 2001;32:377–9.PubMedCrossRef Baltogiannis D, Tasos A, Voutsinas G, Dauaher H, Chambilomatis P, Giannakopoulos X. Bladder cancer mortality in the Epirus district population (Greece). Int Urol Nephrol. 2001;32:377–9.PubMedCrossRef
25.
go back to reference Koffa M, Koumantakis E, Ergazaki M, Tsatsanis C, Spandidos DA. Association of herpesvirus infection with the development of genital cancer. Int J Cancer. 1995;63:58–62.PubMedCrossRef Koffa M, Koumantakis E, Ergazaki M, Tsatsanis C, Spandidos DA. Association of herpesvirus infection with the development of genital cancer. Int J Cancer. 1995;63:58–62.PubMedCrossRef
26.
go back to reference Chuang KL, Pang ST, Liao SK, Wu CT, Chang YH, Chuang HC, et al. Epstein–Barr virus DNA load in tumour tissues correlates with poor differentiation status in non-muscle invasive urothelial carcinomas. BJU Int. 2011;107:150–4.PubMedCrossRef Chuang KL, Pang ST, Liao SK, Wu CT, Chang YH, Chuang HC, et al. Epstein–Barr virus DNA load in tumour tissues correlates with poor differentiation status in non-muscle invasive urothelial carcinomas. BJU Int. 2011;107:150–4.PubMedCrossRef
27.
go back to reference Gazzaniga P, Vercillo R, Gradilone A, Silvestri I, Gandini O, Napolitano M, et al. Prevalence of papillomavirus, Epstein–Barr virus, cytomegalovirus, and herpes simplex virus type 2 in urinary bladder cancer. J Med Virol. 1998;55:262–7.PubMedCrossRef Gazzaniga P, Vercillo R, Gradilone A, Silvestri I, Gandini O, Napolitano M, et al. Prevalence of papillomavirus, Epstein–Barr virus, cytomegalovirus, and herpes simplex virus type 2 in urinary bladder cancer. J Med Virol. 1998;55:262–7.PubMedCrossRef
28.
go back to reference Polesel J, Gheit T, Talamini R, Shahzad N, Lenardon O, Sylla B, et al. Urinary human polyomavirus and papillomavirus infection and bladder cancer risk. Br J Cancer. 2012;106:222–6.PubMedCrossRef Polesel J, Gheit T, Talamini R, Shahzad N, Lenardon O, Sylla B, et al. Urinary human polyomavirus and papillomavirus infection and bladder cancer risk. Br J Cancer. 2012;106:222–6.PubMedCrossRef
29.
go back to reference Rollison DE, Sexton WJ, Rodriguez AR, Kang LC, Daniel R, Shah KV. Lack of BK virus DNA sequences in most transitional-cell carcinomas of the bladder. Int J Cancer. 2007;120:1248–51.PubMedCrossRef Rollison DE, Sexton WJ, Rodriguez AR, Kang LC, Daniel R, Shah KV. Lack of BK virus DNA sequences in most transitional-cell carcinomas of the bladder. Int J Cancer. 2007;120:1248–51.PubMedCrossRef
30.
go back to reference Loghavi S, Bose S. Polyomavirus infection and urothelial carcinoma. Diagn Cytopathol. 2011;39:531–5.PubMedCrossRef Loghavi S, Bose S. Polyomavirus infection and urothelial carcinoma. Diagn Cytopathol. 2011;39:531–5.PubMedCrossRef
31.
go back to reference Anwar K, Naiki H, Nakakuki K, Inuzuka M. High frequency of human papillomavirus infection in carcinoma of the urinary bladder. Cancer. 1992;70:1967–73.PubMedCrossRef Anwar K, Naiki H, Nakakuki K, Inuzuka M. High frequency of human papillomavirus infection in carcinoma of the urinary bladder. Cancer. 1992;70:1967–73.PubMedCrossRef
32.
go back to reference Boucher NR, Scholefield JH, Anderson JB. The aetiological significance of human papillomavirus in bladder cancer. Br J Urol. 1996;78:866–9.PubMedCrossRef Boucher NR, Scholefield JH, Anderson JB. The aetiological significance of human papillomavirus in bladder cancer. Br J Urol. 1996;78:866–9.PubMedCrossRef
33.
go back to reference Chang F, Lipponen P, Tervahauta A, Syrjänen S, Syrjänen K. Transitional cell carcinoma of the bladder: failure to demonstrate human papillomavirus deoxyribonucleic acid by in situ hybridization and polymerase chain reaction. J Urol. 1994;152:1429–33.PubMed Chang F, Lipponen P, Tervahauta A, Syrjänen S, Syrjänen K. Transitional cell carcinoma of the bladder: failure to demonstrate human papillomavirus deoxyribonucleic acid by in situ hybridization and polymerase chain reaction. J Urol. 1994;152:1429–33.PubMed
34.
go back to reference Shigehara K, Sasagawa T, Kawaguchi S, Nakashima T, Shimamura M, Maeda Y, et al. Etiologic role of human papillomavirus infection in bladder carcinoma. Cancer. 2011;117:2067–76.PubMedCrossRef Shigehara K, Sasagawa T, Kawaguchi S, Nakashima T, Shimamura M, Maeda Y, et al. Etiologic role of human papillomavirus infection in bladder carcinoma. Cancer. 2011;117:2067–76.PubMedCrossRef
35.
go back to reference 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;204:217–23.PubMedCrossRef 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;204:217–23.PubMedCrossRef
36.
go back to reference Alexander RE, Hu Y, Kum JB, Montironi R, Lopez-Beltran A, Maclennan GT, Idrees MT, Emerson RE, Ulbright TM, Grignon DG, Eble JN, Cheng L. p16 expression is not associated with human papillomavirus in urinary bladder squamous cell carcinoma. Mod Pathol. 2012 Jun 8. doi:10.1038/modpathol.2012.103. Alexander RE, Hu Y, Kum JB, Montironi R, Lopez-Beltran A, Maclennan GT, Idrees MT, Emerson RE, Ulbright TM, Grignon DG, Eble JN, Cheng L. p16 expression is not associated with human papillomavirus in urinary bladder squamous cell carcinoma. Mod Pathol. 2012 Jun 8. doi:10.​1038/​modpathol.​2012.​103.
37.
go back to reference Ben Selma W, Ziadi S, Ben Gacem R, Amara K, Ksiaa F, Hachana M, et al. Investigation of human papillomavirus in bladder cancer in a series of Tunisian patients. Pathol Res Pract. 2010;15:740–3.CrossRef Ben Selma W, Ziadi S, Ben Gacem R, Amara K, Ksiaa F, Hachana M, et al. Investigation of human papillomavirus in bladder cancer in a series of Tunisian patients. Pathol Res Pract. 2010;15:740–3.CrossRef
38.
go back to reference Badawi H, Ahmed H, Ismail A, Diab M, Moubarak M, Badawy A, et al. Role of human papillomavirus types 16, 18, and 52 in recurrent cystitis and urinary bladder cancer among Egyptian patients. Medsc J Med. 2008;10:232. Badawi H, Ahmed H, Ismail A, Diab M, Moubarak M, Badawy A, et al. Role of human papillomavirus types 16, 18, and 52 in recurrent cystitis and urinary bladder cancer among Egyptian patients. Medsc J Med. 2008;10:232.
39.
go back to reference Moonen PM, Bakkers JM, Kiemeney LA, Schalken JA, Melchers WJ, Witjes JA. Human papilloma virus DNA and p53 mutation analysis on bladder washes in relation to clinical outcome of bladder cancer. Eur Urol. 2007;52:464–8.PubMedCrossRef Moonen PM, Bakkers JM, Kiemeney LA, Schalken JA, Melchers WJ, Witjes JA. Human papilloma virus DNA and p53 mutation analysis on bladder washes in relation to clinical outcome of bladder cancer. Eur Urol. 2007;52:464–8.PubMedCrossRef
Metadata
Title
Association of human herpes, papilloma and polyoma virus families with bladder cancer
Authors
Georgios I. Panagiotakis
Danae Papadogianni
Maria N. Chatziioannou
Ismini Lasithiotaki
Dimitrios Delakas
Demetrios A. Spandidos
Publication date
01-02-2013
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 1/2013
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-012-0512-2

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