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Human polyomavirus and human papillomavirus prevalence and viral load in non-malignant tonsillar tissue and tonsillar carcinoma

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Abstract

Human papillomaviruses (HPVs) are an acknowledged cause of a subset of oropharyngeal cancers, especially of tonsillar cancer. Similar to HPV, some human polyomaviruses (HPyVs), such as Merkel cell polyomavirus (MCPyV), have an oncogenic potential. Recently, several novel HPyVs have been discovered. The aim of our study was to determine viral DNA prevalence and viral DNA load of 13 different HPyVs in benign and malignant tonsillar tissue and to compare the data with those found for HPV. A total of 78 biopsies of palatine tonsils with a histologic diagnosis of non-malignant disease (chronic tonsillitis, tonsillar hyperplasia, n = 40) or tonsillar squamous cell carcinoma (n = 38) were included in the study. HPyV DNA prevalence and viral load were determined by virus-specific quantitative real-time PCRs. JCPyV (1/40, 2.5%) and WUPyV (3/40, 7.5%) were only found in non-malignant tonsillar tissue. HPyV7 and HPyV10 were only detected in one (2.6%) and seven (18.4%) of the 38 cancer biopsies, respectively. Both MCPyV (8/38, 21.1 vs. 4/40, 10.0%) and HPyV6 (2/38, 5.3 vs. 1/40, 2.5%) were found more frequently in cancer samples than in non-malignant tissue, but the differences were not significant. BKPyV, KIPyV, TSPyV, HPyV9, STLPyV, HPyV12 and NJPyV were not discovered in any of the samples. HPyV loads found in HPyV DNA-positive biopsies were very low with no difference between non-malignant and malignant samples (median load <0.0001 HPyV DNA copies per beta-globin gene copy, respectively). In contrast to HPyV, high-risk HPV types (HPV16/HPV18) were found significantly more frequently in tonsillar cancers than in non-malignant tonsillar tissue (17/38, 44.7 vs. 2/40, 5.0%, p < 0.001). Furthermore, high-risk HPV DNA loads were significantly higher in the cancer compared to the non-malignant samples (median load 11.861 vs. 7 × 10−6 HPV DNA copies per beta-globin gene copy, p = 0.012). While both HPV and HPyV may persist in tonsillar tissue, our data on HPyV DNA prevalence and load do not support a role of HPyV in tonsillar carcinogenesis, neither alone nor as co-infecting agents of HPV.

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References

  1. Gillison ML, Chaturvedi AK, Anderson WF, Fakhry C (2015) Epidemiology of human papillomavirus-positive head and neck squamous cell carcinoma. J Clin Oncol 33(29):3235–3242. doi:10.1200/JCO.2015.61.6995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hübbers CU, Akgül B (2015) HPV and cancer of the oral cavity. Virulence 6(3):244–248. doi:10.1080/21505594.2014.999570

    Article  PubMed  PubMed Central  Google Scholar 

  3. Young D, Xiao CC, Murphy B, Moore M, Fakhry C, Day TA (2015) Increase in head and neck cancer in younger patients due to human papillomavirus (HPV). Oral Oncol 51(8):727–730. doi:10.1016/j.oraloncology.2015.03.015

    Article  PubMed  Google Scholar 

  4. Gooi Z, Chan JY, Fakhry C (2016) The epidemiology of the human papillomavirus related to oropharyngeal head and neck cancer. Laryngoscope 126(4):894–900. doi:10.1002/lary.25767

    Article  PubMed  Google Scholar 

  5. Ndiaye C, Mena M, Alemany L, Arbyn M, Castellsague X, Laporte L, Bosch FX, de Sanjose S, Trottier H (2014) HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol 15(12):1319–1331. doi:10.1016/S1470-2045(14)70471-1

    Article  CAS  PubMed  Google Scholar 

  6. Deschler DG, Richmon JD, Khariwala SS, Ferris RL, Wang MB (2014) The “new” head and neck cancer patient-young, nonsmoker, nondrinker, and HPV positive: evaluation. Otolaryngol Head Neck Surg 151(3):375–380. doi:10.1177/0194599814538605

    Article  PubMed  PubMed Central  Google Scholar 

  7. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917. doi:10.1002/ijc.25516

    Article  CAS  PubMed  Google Scholar 

  8. RKI (2015) Krebs in Deutschland 2011/2012, 10th edn. Robert Koch Institut, Berlin

    Google Scholar 

  9. Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, Forastiere A, Gillison ML (2008) Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst 100(4):261–269. doi:10.1093/jnci/djn011

    Article  CAS  PubMed  Google Scholar 

  10. Rosenthal DI, Harari PM, Giralt J, Bell D, Raben D, Liu J, Schulten J, Ang KK, Bonner JA (2016) Association of human papillomavirus and p16 status with outcomes in the IMCL-9815 phase III registration trial for patients with locoregionally advanced oropharyngeal squamous cell carcinoma of the head and neck treated with radiotherapy with or without cetuximab. J Clin Oncol 34(12):1300–1308. doi:10.1200/JCO.2015.62.5970

    Article  CAS  PubMed  Google Scholar 

  11. Tinhofer I, Johrens K, Keilholz U, Kaufmann A, Lehmann A, Weichert W, Stenzinger A, Stromberger C, Klinghammer K, Becker ET, Dommerich S, Stolzel K, Hofmann VM, Hildebrandt B, Moser L, Ervens J, Bottcher A, Albers A, Stabenow R, Reinecke A, Budach V, Hoffmeister B, Raguse JD (2015) Contribution of human papilloma virus to the incidence of squamous cell carcinoma of the head and neck in a European population with high smoking prevalence. Eur J Cancer 51(4):514–521. doi:10.1016/j.ejca.2014.12.018

    Article  CAS  PubMed  Google Scholar 

  12. Sedghizadeh PP, Billington WD, Paxton D, Ebeed R, Mahabady S, Clark GT, Enciso R (2016) Is p16-positive oropharyngeal squamous cell carcinoma associated with favorable prognosis? A systematic review and meta-analysis. Oral Oncol 54:15–27. doi:10.1016/j.oraloncology.2016.01.002

    Article  PubMed  Google Scholar 

  13. Guo T, Eisele DW, Fakhry C (2016) The potential impact of prophylactic human papillomavirus vaccination on oropharyngeal cancer. Cancer. doi:10.1002/cncr.29992

    Google Scholar 

  14. Starr P (2015) Encouraging results for pembrolizumab in head and neck cancer. Am Health Drug Benefits 8(Spec Issue):16

    PubMed  PubMed Central  Google Scholar 

  15. DeCaprio JA, Garcea RL (2013) A cornucopia of human polyomaviruses. Nat Rev Microbiol 11(4):264–276. doi:10.1038/nrmicro2992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ehlers B, Wieland U (2013) The novel human polyomaviruses HPyV6, 7, 9 and beyond. APMIS 121(8):783–795. doi:10.1111/apm.12104

    Article  CAS  PubMed  Google Scholar 

  17. Feltkamp MC, Kazem S, van der Meijden E, Lauber C, Gorbalenya AE (2013) From Stockholm to Malawi: recent developments in studying human polyomaviruses. J Gen Virol 94(Pt 3):482–496. doi:10.1099/vir.0.048462-0

    Article  CAS  PubMed  Google Scholar 

  18. Mishra N, Pereira M, Rhodes RH, An P, Pipas JM, Jain K, Kapoor A, Briese T, Faust PL, Lipkin WI (2014) Identification of a novel polyomavirus in a pancreatic transplant recipient with retinal blindness and vasculitic myopathy. J Infect Dis 210(10):1595–1599. doi:10.1093/infdis/jiu250

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gossai A, Waterboer T, Nelson HH, Michel A, Willhauck-Fleckenstein M, Farzan SF, Hoen AG, Christensen BC, Kelsey KT, Marsit CJ, Pawlita M, Karagas MR (2016) Seroepidemiology of human polyomaviruses in a US population. Am J Epidemiol 183(1):61–69. doi:10.1093/aje/kwv155

    Article  PubMed  Google Scholar 

  20. Kean JM, Rao S, Wang M, Garcea RL (2009) Seroepidemiology of human polyomaviruses. PLoS Pathog 5(3):e1000363. doi:10.1371/journal.ppat.1000363

    Article  PubMed  PubMed Central  Google Scholar 

  21. Nicol JT, Robinot R, Carpentier A, Carandina G, Mazzoni E, Tognon M, Touze A, Coursaget P (2013) Age-specific seroprevalences of merkel cell polyomavirus, human polyomaviruses 6, 7, and 9, and trichodysplasia spinulosa-associated polyomavirus. Clin Vaccine Immunol 20(3):363–368. doi:10.1128/CVI.00438-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sadeghi M, Aaltonen LM, Hedman L, Chen T, Soderlund-Venermo M, Hedman K (2014) Detection of TS polyomavirus DNA in tonsillar tissues of children and adults: evidence for site of viral latency. J Clin Virol 59(1):55–58. doi:10.1016/j.jcv.2013.11.008

    Article  CAS  PubMed  Google Scholar 

  23. Akhgari S, Mohraz M, Azadmanesh K, Vahabpour R, Kazemimanesh M, Aghakhani A, Jozpanahi M, Banifazl M, Bavand A, Ramezani A (2016) Frequency and subtype of BK virus infection in Iranian patients infected with HIV. Med Microbiol Immunol 205(1):57–62. doi:10.1007/s00430-015-0426-x

    Article  CAS  PubMed  Google Scholar 

  24. Hirsch HH, Kardas P, Kranz D, Leboeuf C (2013) The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS 121(8):685–727. doi:10.1111/apm.12128

    Article  CAS  PubMed  Google Scholar 

  25. Rinaldo CH, Tylden GD, Sharma BN (2013) The human polyomavirus BK (BKPyV): virological background and clinical implications. APMIS 121(8):728–745. doi:10.1111/apm.12134

    Article  CAS  PubMed  Google Scholar 

  26. Teutsch K, Schweitzer F, Knops E, Kaiser R, Pfister H, Verheyen J, Gobel H, Cingoz T, Di Cristanziano V (2015) Early identification of renal transplant recipients with high risk of polyomavirus-associated nephropathy. Med Microbiol Immunol 204(6):657–664. doi:10.1007/s00430-015-0398-x

    Article  CAS  PubMed  Google Scholar 

  27. Feng H, Shuda M, Chang Y, Moore PS (2008) Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319(5866):1096–1100. doi:10.1126/science.1152586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Shuda M, Arora R, Kwun HJ, Feng H, Sarid R, Fernandez-Figueras MT, Tolstov Y, Gjoerup O, Mansukhani MM, Swerdlow SH, Chaudhary PM, Kirkwood JM, Nalesnik MA, Kant JA, Weiss LM, Moore PS, Chang Y (2009) Human Merkel cell polyomavirus infection I. MCV T antigen expression in Merkel cell carcinoma, lymphoid tissues and lymphoid tumors. Int J Cancer 125(6):1243–1249. doi:10.1002/ijc.24510

    Article  CAS  PubMed  Google Scholar 

  29. Ho J, Jedrych JJ, Feng H, Natalie AA, Grandinetti L, Mirvish E, Crespo MM, Yadav D, Fasanella KE, Proksell S, Kuan SF, Pastrana DV, Buck CB, Shuda Y, Moore PS, Chang Y (2015) Human polyomavirus 7-associated pruritic rash and viremia in transplant recipients. J Infect Dis 211(10):1560–1565. doi:10.1093/infdis/jiu524

    Article  PubMed  Google Scholar 

  30. Kazem S, van der Meijden E, Feltkamp MC (2013) The trichodysplasia spinulosa-associated polyomavirus: virological background and clinical implications. APMIS 121(8):770–782. doi:10.1111/apm.12092

    Article  CAS  PubMed  Google Scholar 

  31. Buck CB, Phan GQ, Raiji MT, Murphy PM, McDermott DH, McBride AA (2012) Complete genome sequence of a tenth human polyomavirus. J Virol 86(19):10887. doi:10.1128/JVI.01690-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Korup S, Rietscher J, Calvignac-Spencer S, Trusch F, Hofmann J, Moens U, Sauer I, Voigt S, Schmuck R, Ehlers B (2013) Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS ONE 8(3):e58021. doi:10.1371/journal.pone.0058021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lim ES, Reyes A, Antonio M, Saha D, Ikumapayi UN, Adeyemi M, Stine OC, Skelton R, Brennan DC, Mkakosya RS, Manary MJ, Gordon JI, Wang D (2013) Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology 436(2):295–303. doi:10.1016/j.virol.2012.12.005

    Article  CAS  PubMed  Google Scholar 

  34. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB (2010) Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 7(6):509–515. doi:10.1016/j.chom.2010.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Scuda N, Hofmann J, Calvignac-Spencer S, Ruprecht K, Liman P, Kuhn J, Hengel H, Ehlers B (2011) A novel human polyomavirus closely related to the african green monkey-derived lymphotropic polyomavirus. J Virol 85(9):4586–4590. doi:10.1128/JVI.02602-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Siebrasse EA, Reyes A, Lim ES, Zhao G, Mkakosya RS, Manary MJ, Gordon JI, Wang D (2012) Identification of MW polyomavirus, a novel polyomavirus in human stool. J Virol 86(19):10321–10326. doi:10.1128/JVI.01210-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Yu G, Greninger AL, Isa P, Phan TG, Martinez MA, de la Luz Sanchez M, Contreras JF, Santos-Preciado JI, Parsonnet J, Miller S, DeRisi JL, Delwart E, Arias CF, Chiu CY (2012) Discovery of a novel polyomavirus in acute diarrheal samples from children. PLoS ONE 7(11):e49449. doi:10.1371/journal.pone.0049449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Falcone V, Ridder GJ, Panning M, Bierbaum S, Neumann-Haefelin D, Huzly D (2011) Human bocavirus DNA in paranasal sinus mucosa. Emerg Infect Dis 17(8):1564–1565. doi:10.3201/eid1708.101944

    PubMed  PubMed Central  Google Scholar 

  39. Wieland U, Silling S, Hellmich M, Potthoff A, Pfister H, Kreuter A (2014) Human polyomaviruses 6, 7, 9, 10 and Trichodysplasia spinulosa-associated polyomavirus in HIV-infected men. J Gen Virol 95(Pt 4):928–932. doi:10.1099/vir.0.061259-0

    Article  CAS  PubMed  Google Scholar 

  40. Wieland U, Hellmich M, Wetendorf J, Potthoff A, Hofler D, Swoboda J, Fuchs W, Brockmeyer N, Pfister H, Kreuter A (2015) Smoking and anal high-risk human papillomavirus DNA loads in HIV-positive men who have sex with men. Int J Med Microbiol 305(7):689–696. doi:10.1016/j.ijmm.2015.08.019

    Article  PubMed  Google Scholar 

  41. Sihto H, Kukko H, Koljonen V, Sankila R, Bohling T, Joensuu H (2009) Clinical factors associated with Merkel cell polyomavirus infection in Merkel cell carcinoma. J Natl Cancer Inst 101(13):938–945. doi:10.1093/jnci/djp139

    Article  CAS  PubMed  Google Scholar 

  42. Schmitt M, Bravo IG, Snijders PJ, Gissmann L, Pawlita M, Waterboer T (2006) Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 44(2):504–512. doi:10.1128/JCM.44.2.504-512.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Silling S, Kreuter A, Hellmich M, Swoboda J, Pfister H, Wieland U (2012) Human papillomavirus oncogene mRNA testing for the detection of anal dysplasia in HIV-positive men who have sex with men. J Clin Virol 53(4):325–331. doi:10.1016/j.jcv.2011.12.029

    Article  CAS  PubMed  Google Scholar 

  44. IARC (2012) Monographs on the evaluation of carcinogenic risks to humans. Biological agents. A review of human carcinogens., vol 100B. Lyon

  45. van Duin M, Snijders PJ, Schrijnemakers HF, Voorhorst FJ, Rozendaal L, Nobbenhuis MA, van den Brule AJ, Verheijen RH, Helmerhorst TJ, Meijer CJ (2002) Human papillomavirus 16 load in normal and abnormal cervical scrapes: an indicator of CIN II/III and viral clearance. Int J Cancer 98(4):590–595

    Article  PubMed  Google Scholar 

  46. Wieland U, Silling S, Scola N, Potthoff A, Gambichler T, Brockmeyer NH, Pfister H, Kreuter A (2011) Merkel cell polyomavirus infection in HIV-positive men. Arch Dermatol 147(4):401–406. doi:10.1001/archdermatol.2011.42

    Article  PubMed  Google Scholar 

  47. Karachaliou M, Waterboer T, Casabonne D, Chalkiadaki G, Roumeliotaki T, Michel A, Stiakaki E, Chatzi L, Pawlita M, Kogevinas M, de Sanjose S (2016) The natural history of human polyomaviruses and herpesviruses in early life-the Rhea birth cohort in Greece. Am J Epidemiol 183(7):671–679. doi:10.1093/aje/kwv281

    Article  PubMed  Google Scholar 

  48. Salakova M, Koslabova E, Vojtechova Z, Tachezy R, Sroller V (2016) Detection of human polyomaviruses MCPyV, HPyV6, and HPyV7 in malignant and non-malignant tonsillar tissues. J Med Virol 88(4):695–702. doi:10.1002/jmv.24385

    Article  CAS  PubMed  Google Scholar 

  49. Astegiano S, Terlizzi ME, Elia M, Cavallo GP, Costa C, Cavallo R, Bergallo M (2010) Prevalence of polyomaviruses BK, JC, SV40, KI, and WU in non-malignant tonsil specimens. Minerva Med 101(6):385–389

    CAS  PubMed  Google Scholar 

  50. Babakir-Mina M, Ciccozzi M, Bonifacio D, Bergallo M, Costa C, Cavallo R, Di Bonito L, Perno CF, Ciotti M (2009) Identification of the novel KI and WU polyomaviruses in human tonsils. J Clin Virol 46(1):75–79. doi:10.1016/j.jcv.2009.06.009

    Article  CAS  PubMed  Google Scholar 

  51. Comar M, Zanotta N, Bovenzi M, Campello C (2010) JCV/BKV and SV40 viral load in lymphoid tissues of young immunocompetent children from an area of north-east Italy. J Med Virol 82(7):1236–1240. doi:10.1002/jmv.21786

    Article  PubMed  Google Scholar 

  52. Comar M, Zanotta N, Rossi T, Pelos G, D’Agaro P (2011) Secondary lymphoid tissue as an important site for WU polyomavirus infection in immunocompetent children. J Med Virol 83(8):1446–1450. doi:10.1002/jmv.22124

    Article  PubMed  Google Scholar 

  53. Monaco MC, Jensen PN, Hou J, Durham LC, Major EO (1998) Detection of JC virus DNA in human tonsil tissue: evidence for site of initial viral infection. J Virol 72(12):9918–9923

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Kato A, Kitamura T, Takasaka T, Tominaga T, Ishikawa A, Zheng HY, Yogo Y (2004) Detection of the archetypal regulatory region of JC virus from the tonsil tissue of patients with tonsillitis and tonsilar hypertrophy. J Neurovirol 10(4):244–249. doi:10.1080/13550280490468663

    Article  CAS  PubMed  Google Scholar 

  55. Sahiner F, Gumral R, Yildizoglu U, Babayigit MA, Durmaz A, Yigit N, Saracli MA, Kubar A (2014) Coexistence of Epstein–Barr virus and Parvovirus B19 in tonsillar tissue samples: quantitative measurement by real-time PCR. Int J Pediatr Otorhinolaryngol 78(8):1288–1293. doi:10.1016/j.ijporl.2014.05.012

    Article  PubMed  Google Scholar 

  56. Ryschkewitsch C, Jensen P, Hou J, Fahle G, Fischer S, Major EO (2004) Comparison of PCR-southern hybridization and quantitative real-time PCR for the detection of JC and BK viral nucleotide sequences in urine and cerebrospinal fluid. J Virol Methods 121(2):217–221. doi:10.1016/j.jviromet.2004.06.021

    Article  CAS  PubMed  Google Scholar 

  57. Günel C, Kirdar S, Omurlu IK, Agdas F (2015) Detection of the Epstein–Barr virus, human bocavirus and novel KI and KU polyomaviruses in adenotonsillar tissues. Int J Pediatr Otorhinolaryngol 79(3):423–427. doi:10.1016/j.ijporl.2015.01.007

    Article  PubMed  Google Scholar 

  58. Bergallo M, Terlizzi ME, Astegiano S, Ciotti M, Babakir-Mina M, Perno CF, Cavallo R, Costa C (2009) Real time PCR TaqMan assays for detection of polyomaviruses KIV and WUV in clinical samples. J Virol Methods 162(1–2):69–74. doi:10.1016/j.jviromet.2009.07.016

    Article  CAS  PubMed  Google Scholar 

  59. Papadimitriou JC, Randhawa P, Rinaldo CH, Drachenberg CB, Alexiev B, Hirsch HH (2016) BK polyomavirus infection and renourinary tumorigenesis. Am J Transpl 16(2):398–406. doi:10.1111/ajt.13550

    Article  CAS  Google Scholar 

  60. Kantola K, Sadeghi M, Lahtinen A, Koskenvuo M, Aaltonen LM, Mottonen M, Rahiala J, Saarinen-Pihkala U, Riikonen P, Jartti T, Ruuskanen O, Soderlund-Venermo M, Hedman K (2009) Merkel cell polyomavirus DNA in tumor-free tonsillar tissues and upper respiratory tract samples: implications for respiratory transmission and latency. J Clin Virol 45(4):292–295. doi:10.1016/j.jcv.2009.04.008

    Article  CAS  PubMed  Google Scholar 

  61. Peng J, Li K, Zhang C, Jin Q (2016) MW polyomavirus and STL polyomavirus present in tonsillar tissues from children with chronic tonsillar disease. Clin Microbiol Infect 22(1):97.e1–3. doi:10.1016/j.cmi.2015.08.028

    Article  Google Scholar 

  62. Schmitt M, Wieland U, Kreuter A, Pawlita M (2012) C-terminal deletions of Merkel cell polyomavirus large T-antigen, a highly specific surrogate marker for virally induced malignancy. Int J Cancer 131(12):2863–2868. doi:10.1002/ijc.27607

    Article  CAS  PubMed  Google Scholar 

  63. Wieland U, Scola N, Stolte B, Stucker M, Silling S, Kreuter A (2012) No evidence for a causal role of Merkel cell polyomavirus in keratoacanthoma. J Am Acad Dermatol 67(1):41–46. doi:10.1016/j.jaad.2011.07.026

    Article  PubMed  Google Scholar 

  64. Josefsson AM, Magnusson PK, Ylitalo N, Sorensen P, Qwarforth-Tubbin P, Andersen PK, Melbye M, Adami HO, Gyllensten UB (2000) Viral load of human papilloma virus 16 as a determinant for development of cervical carcinoma in situ: a nested case-control study. Lancet 355(9222):2189–2193. doi:10.1016/S0140-6736(00)02401-6

    Article  CAS  PubMed  Google Scholar 

  65. Sundström K, Ploner A, Dahlstrom LA, Palmgren J, Dillner J, Adami HO, Ylitalo N, Sparen P (2013) Prospective study of HPV16 viral load and risk of in situ and invasive squamous cervical cancer. Cancer Epidemiol Biomarkers Prev 22(1):150–158. doi:10.1158/1055-9965.EPI-12-0953-T

    Article  PubMed  Google Scholar 

  66. Rödel F, Wieland U, Fraunholz I, Kitz J, Rave-Frank M, Wolff HA, Weiss C, Wirtz R, Balermpas P, Fokas E, Rodel C (2015) Human papillomavirus DNA load and p16INK4a expression predict for local control in patients with anal squamous cell carcinoma treated with chemoradiotherapy. Int J Cancer 136(2):278–288. doi:10.1002/ijc.28979

    Article  PubMed  Google Scholar 

  67. Nakamura T, Sato Y, Watanabe D, Ito H, Shimonohara N, Tsuji T, Nakajima N, Suzuki Y, Matsuo K, Nakagawa H, Sata T, Katano H (2010) Nuclear localization of Merkel cell polyomavirus large T antigen in Merkel cell carcinoma. Virology 398(2):273–279. doi:10.1016/j.virol.2009.12.024

    Article  CAS  PubMed  Google Scholar 

  68. Kreuter A, Silling S, Dewan M, Stucker M, Wieland U (2011) Evaluation of 4 recently discovered human polyomaviruses in primary cutaneous B-cell and T-cell lymphoma. Arch Dermatol 147(12):1449–1451. doi:10.1001/archdermatol.2011.330

    Article  PubMed  Google Scholar 

  69. Scola N, Wieland U, Silling S, Altmeyer P, Stucker M, Kreuter A (2012) Prevalence of human polyomaviruses in common and rare types of non-Merkel cell carcinoma skin cancer. Br J Dermatol 167(6):1315–1320. doi:10.1111/j.1365-2133.2012.11141.x

    Article  CAS  PubMed  Google Scholar 

  70. D’Souza G, Kreimer AR, Viscidi R, Pawlita M, Fakhry C, Koch WM, Westra WH, Gillison ML (2007) Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 356(19):1944–1956. doi:10.1056/NEJMoa065497

    Article  PubMed  Google Scholar 

  71. Rietbergen MM, Leemans CR, Bloemena E, Heideman DA, Braakhuis BJ, Hesselink AT, Witte BI, Baatenburg de Jong RJ, Meijer CJ, Snijders PJ, Brakenhoff RH (2013) Increasing prevalence rates of HPV attributable oropharyngeal squamous cell carcinomas in the Netherlands as assessed by a validated test algorithm. Int J Cancer 132(7):1565–1571. doi:10.1002/ijc.27821

    Article  CAS  PubMed  Google Scholar 

  72. Chen R, Sehr P, Waterboer T, Leivo I, Pawlita M, Vaheri A, Aaltonen LM (2005) Presence of DNA of human papillomavirus 16 but no other types in tumor-free tonsillar tissue. J Clin Microbiol 43(3):1408–1410. doi:10.1128/JCM.43.3.1408-1410.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Klussmann JP, Weissenborn SJ, Wieland U, Dries V, Kolligs J, Jungehuelsing M, Eckel HE, Dienes HP, Pfister HJ, Fuchs PG (2001) Prevalence, distribution, and viral load of human papillomavirus 16 DNA in tonsillar carcinomas. Cancer 92(11):2875–2884

    Article  CAS  PubMed  Google Scholar 

  74. Zheng Y, Xia P, Zheng HC, Takahashi H, Masuda S, Takano Y (2010) The screening of viral risk factors in tongue and pharyngolaryngeal squamous carcinoma. Anticancer Res 30(4):1233–1238

    CAS  PubMed  Google Scholar 

  75. Mooren JJ, Gultekin SE, Straetmans JM, Haesevoets A, Peutz-Kootstra CJ, Huebbers CU, Dienes HP, Wieland U, Ramaekers FC, Kremer B, Speel EJ, Klussmann JP (2014) P16(INK4A) immunostaining is a strong indicator for high-risk-HPV-associated oropharyngeal carcinomas and dysplasias, but is unreliable to predict low-risk-HPV-infection in head and neck papillomas and laryngeal dysplasias. Int J Cancer 134(9):2108–2117. doi:10.1002/ijc.28534

    Article  CAS  PubMed  Google Scholar 

  76. Stanley M (2014) HPV vaccination in boys and men. Hum Vaccin Immunother 10(7):2109–2111. doi:10.4161/hv.29137

    Article  PubMed  PubMed Central  Google Scholar 

  77. Herrero R, Quint W, Hildesheim A, Gonzalez P, Struijk L, Katki HA, Porras C, Schiffman M, Rodriguez AC, Solomon D, Jimenez S, Schiller JT, Lowy DR, van Doorn LJ, Wacholder S, Kreimer AR, Group CVTV (2013) Reduced prevalence of oral human papillomavirus (HPV) 4 years after bivalent HPV vaccination in a randomized clinical trial in Costa Rica. PLoS ONE 8(7):e68329. doi:10.1371/journal.pone.0068329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Grün N, Ahrlund-Richter A, Franzen J, Mirzaie L, Marions L, Ramqvist T, Dalianis T (2015) Oral human papillomavirus (HPV) prevalence in youth and cervical HPV prevalence in women attending a youth clinic in Sweden, a follow up-study 2013-2014 after gradual introduction of public HPV vaccination. Infect Dis (Lond) 47(1):57–61. doi:10.3109/00365548.2014.964764

    Article  Google Scholar 

  79. Boscolo-Rizzo P, Pawlita M, Holzinger D (2016) From HPV-positive towards HPV-driven oropharyngeal squamous cell carcinomas. Cancer Treat Rev 42:24–29. doi:10.1016/j.ctrv.2015.10.009

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  81. Moens U, Van Ghelue M, Ehlers B (2014) Are human polyomaviruses co-factors for cancers induced by other oncoviruses? Rev Med Virol 24(5):343–360. doi:10.1002/rmv.1798

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Monika Junk and Nabila Ristow for excellent technical assistance. This work was supported by the German Federal Ministry of Health (German National Reference Center for Papilloma- and Polyomaviruses, Grant No. 1369-401).

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Correspondence to Baki Akgül.

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Herberhold, S., Hellmich, M., Panning, M. et al. Human polyomavirus and human papillomavirus prevalence and viral load in non-malignant tonsillar tissue and tonsillar carcinoma. Med Microbiol Immunol 206, 93–103 (2017). https://doi.org/10.1007/s00430-016-0486-6

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  • DOI: https://doi.org/10.1007/s00430-016-0486-6

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