1887

Abstract

The prevalence of 13 polyomaviruses (PyVs) in the tonsil brushings and gargles of immunocompetent children and adults was assessed. Patients undergoing tonsillectomy for benign indications were recruited in 19 centres in France. After resection, the entire outer surface of the right and left halves of the tonsils was brushed extensively. Gargles were also collected prior to surgery in selected adults. A species-specific multiplex assay was used to detect the DNA of 13 PyVs. In tonsil brushings (n=689), human PyV 6 (HPyV6) and Merkel cell PyV (MCPyV) were the most prevalent (≈15 %), followed by trichodysplasia spinulosa-associated PyV (TSPyV), BKPyV, Washington University PyV (WUPyV) and human PyV 9 (HPyV9) (1 to 5 %), and human PyV 7 (HPyV7), John Cunningham PyV (JCPyV) and Simian virus 40 (SV40) (<1 %), while no Karolinska Institute PyV (KIPyV), Malawi PyV (MWPyV), human PyV 12 (HPyV12) or Lyon IARC PyV (LIPyV) were detected. The prevalence of TSPyV and BKPyV was significantly higher in children versus adults, whereas for HPyV6 the opposite was found. HPyV6 and WUPyV were significantly more prevalent in men versus women. In gargles (n=139), MCPyV was the most prevalent (≈40 %), followed by HPyV6, HPyV9 and LIPyV (2 to 4 %), and then BKPyV (≈1 %), while other PyVs were not detected. MCPyV and LIPyV were significantly more prevalent in gargles compared to tonsil brushings, in contrast to HPyV6. We described differing patterns of individual PyV infections in tonsils and gargles in a large age-stratified population. Comparison of the spectrum of PyVs in paired tonsil samples and gargles adds to the current knowledge on PyV epidemiology, contributing towards a better understanding of PyV acquisition and transmission and its potential role in head and neck diseases.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001156
2018-11-08
2024-12-02
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/12/1686.html?itemId=/content/journal/jgv/10.1099/jgv.0.001156&mimeType=html&fmt=ahah

References

  1. Bennett J, Dolin R, Mandell BM. Douglas, and Bennett's Principles and Practice of Infectious Diseases, 8th ed. vol. 1 Philadelphia, PA: Elsevier Saunders; 2015
    [Google Scholar]
  2. Dalianis T, Hirsch HH. Human polyomaviruses in disease and cancer. Virology 2013; 437:63–72 [View Article][PubMed]
    [Google Scholar]
  3. Gheit T, Dutta S, Oliver J, Robitaille A, Hampras S et al. Isolation and characterization of a novel putative human polyomavirus. Virology 2017; 506:45–54 [View Article][PubMed]
    [Google Scholar]
  4. Astegiano S, Terlizzi ME, Elia M, Cavallo GP, Costa C et al. Prevalence of polyomaviruses BK, JC, SV40, KI, and WU in non-malignant tonsil specimens. Minerva Med 2010; 101:385–389[PubMed]
    [Google Scholar]
  5. Hirsch HH, Babel N, Comoli P, Friman V, Ginevri F et al. European perspective on human polyomavirus infection, replication and disease in solid organ transplantation. Clin Microbiol Infect 2014; 20:74–88 [View Article][PubMed]
    [Google Scholar]
  6. Hirsch HH, Kardas P, Kranz D, Leboeuf C. The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS 2017; 121:685–727 [View Article][PubMed]
    [Google Scholar]
  7. Nickeleit V, Hirsch HH, Binet IF, Gudat F, Prince O et al. Polyomavirus infection of renal allograft recipients: from latent infection to manifest disease. J Am Soc Nephrol 1999; 10:1080–1089[PubMed]
    [Google Scholar]
  8. de Gascun CF, Carr MJ. Human polyomavirus reactivation: disease pathogenesis and treatment approaches. Clin Dev Immunol 2013; 2013:1–27 [View Article][PubMed]
    [Google Scholar]
  9. IARC Malaria and Some Polyomaviruses (SV40, BK, JC, and Merkel Cell Viruses). IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, No. 104 2014 pp. 1–353 http://monographs.iarc.fr/ENG/Monographs/vol104/index.php [accessed 6 April 2018]
    [Google Scholar]
  10. Viscidi RP, Rollison DE, Sondak VK, Silver B, Messina JL et al. Age-specific seroprevalence of Merkel cell polyomavirus, BK virus, and JC virus. Clin Vaccine Immunol 2011; 18:1737–1743 [View Article][PubMed]
    [Google Scholar]
  11. Sroller V, Hamšíková E, Ludvíková V, Vochozková P, Kojzarová M et al. Seroprevalence rates of BKV, JCV, and MCPyV polyomaviruses in the general Czech Republic population. J Med Virol 2014; 86:1560–1568 [View Article][PubMed]
    [Google Scholar]
  12. Kean JM, Rao S, Wang M, Garcea RL. Seroepidemiology of human polyomaviruses. PLoS Pathog 2009; 5:e1000363 [View Article][PubMed]
    [Google Scholar]
  13. Šroller V, Hamšíková E, Ludvíková V, Musil J, Němečková Š et al. Seroprevalence rates of HPyV6, HPyV7, TSPyV, HPyV9, MWPyV and KIPyV polyomaviruses among the healthy blood donors. J Med Virol 2016; 88:1254–1261 [View Article][PubMed]
    [Google Scholar]
  14. Nicol JT, Robinot R, Carpentier A, Carandina G, Mazzoni E et al. Age-specific seroprevalences of merkel cell polyomavirus, human polyomaviruses 6, 7, and 9, and trichodysplasia spinulosa-associated polyomavirus. Clin Vaccine Immunol 2013; 20:363–368 [View Article][PubMed]
    [Google Scholar]
  15. van der Meijden E, Bialasiewicz S, Rockett RJ, Tozer SJ, Sloots TP et al. Different serologic behavior of MCPyV, TSPyV, HPyV6, HPyV7 and HPyV9 polyomaviruses found on the skin. PLoS One 2013; 8:e81078 [View Article][PubMed]
    [Google Scholar]
  16. Gossai A, Waterboer T, Nelson HH, Michel A, Willhauck-Fleckenstein M et al. Seroepidemiology of Human Polyomaviruses in a US Population. Am J Epidemiol 2016; 183:61–69 [View Article][PubMed]
    [Google Scholar]
  17. Carter JJ, Paulson KG, Wipf GC, Miranda D, Madeleine MM et al. Association of Merkel cell polyomavirus-specific antibodies with Merkel cell carcinoma. J Natl Cancer Inst 2009; 101:1510–1522 [View Article][PubMed]
    [Google Scholar]
  18. Mancuso G, Antona J, Sirini C, Salvo M, Giacometti L et al. Frequent detection of Merkel cell polyomavirus DNA in tissues from 10 consecutive autopsies. J Gen Virol 2017; 98:1372–1376 [View Article][PubMed]
    [Google Scholar]
  19. Saláková M, Košlabová E, Vojtěchová Z, Tachezy R, Šroller V. Detection of human polyomaviruses MCPyV, HPyV6, and HPyV7 in malignant and non-malignant tonsillar tissues. J Med Virol 2016; 88:695–702 [View Article][PubMed]
    [Google Scholar]
  20. Sadeghi M, Wang Y, Ramqvist T, Aaltonen LM, Pyöriä L et al. Multiplex detection in tonsillar tissue of all known human polyomaviruses. BMC Infect Dis 2017; 17:409 [View Article][PubMed]
    [Google Scholar]
  21. Peng J, Li K, Zhang C, Jin Q. MW polyomavirus and STL polyomavirus present in tonsillar tissues from children with chronic tonsillar disease. Clin Microbiol Infect 2016; 22:97.e1–97.e3 [View Article][PubMed]
    [Google Scholar]
  22. Loyo M, Guerrero-Preston R, Brait M, Hoque MO, Chuang A et al. Quantitative detection of Merkel cell virus in human tissues and possible mode of transmission. Int J Cancer 2010; 126:2991–2996 [View Article][PubMed]
    [Google Scholar]
  23. Foulongne V, Courgnaud V, Champeau W, Segondy M. Detection of Merkel cell polyomavirus on environmental surfaces. J Med Virol 2011; 83:1435–1439 [View Article][PubMed]
    [Google Scholar]
  24. Martel-Jantin C, Pedergnana V, Nicol JT, Leblond V, Trégouët DA et al. Merkel cell polyomavirus infection occurs during early childhood and is transmitted between siblings. J Clin Virol 2013; 58:288–291 [View Article][PubMed]
    [Google Scholar]
  25. Nguyen KD, Lee EE, Yue Y, Stork J, Pock L et al. Human polyomavirus 6 and 7 are associated with pruritic and dyskeratotic dermatoses. J Am Acad Dermatol 2017; 76:932–940 [View Article][PubMed]
    [Google Scholar]
  26. Schowalter RM, Pastrana DV, Pumphrey KA, Moyer AL, Buck CB. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 2010; 7:509–515 [View Article][PubMed]
    [Google Scholar]
  27. Herberhold S, Hellmich M, Panning M, Bartok E, Silling S et al. Human polyomavirus and human papillomavirus prevalence and viral load in non-malignant tonsillar tissue and tonsillar carcinoma. Med Microbiol Immunol 2017; 206:93–103 [View Article][PubMed]
    [Google Scholar]
  28. Franceschi S, Combes JD, Dalstein V, Caudroy S, Clifford G et al. Deep brush-based cytology in tonsils resected for benign diseases. Int J Cancer 2015; 137:2994–2999 [View Article][PubMed]
    [Google Scholar]
  29. Sadeghi M, Aaltonen LM, Hedman L, Chen T, Söderlund-Venermo M et al. Detection of TS polyomavirus DNA in tonsillar tissues of children and adults: evidence for site of viral latency. J Clin Virol 2014; 59:55–58 [View Article][PubMed]
    [Google Scholar]
  30. Chen T, Mattila PS, Jartti T, Ruuskanen O, Söderlund-Venermo M et al. Seroepidemiology of the newly found trichodysplasia spinulosa-associated polyomavirus. J Infect Dis 2011; 204:1523–1526 [View Article][PubMed]
    [Google Scholar]
  31. van der Meijden E, Kazem S, Burgers MM, Janssens R, Bouwes Bavinck JN et al. Seroprevalence of trichodysplasia spinulosa-associated polyomavirus. Emerg Infect Dis 2011; 17:1355–1363 [View Article][PubMed]
    [Google Scholar]
  32. Knowles WA, Pipkin P, Andrews N, Vyse A, Minor P et al. Population-based study of antibody to the human polyomaviruses BKV and JCV and the simian polyomavirus SV40. J Med Virol 2003; 71:115–123 [View Article][PubMed]
    [Google Scholar]
  33. Egli A, Infanti L, Dumoulin A, Buser A, Samaridis J et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis 2009; 199:837–846 [View Article][PubMed]
    [Google Scholar]
  34. Antonsson A, Green AC, Mallitt KA, O'Rourke PK, Pawlita M et al. Prevalence and stability of antibodies to the BK and JC polyomaviruses: a long-term longitudinal study of Australians. J Gen Virol 2010; 91:1849–1853 [View Article][PubMed]
    [Google Scholar]
  35. Babakir-Mina M, Ciccozzi M, Bonifacio D, Bergallo M, Costa C et al. Identification of the novel KI and WU polyomaviruses in human tonsils. J Clin Virol 2009; 46:75–79 [View Article][PubMed]
    [Google Scholar]
  36. Ho J, Jedrych JJ, Feng H, Natalie AA, Grandinetti L et al. Human polyomavirus 7-associated pruritic rash and viremia in transplant recipients. J Infect Dis 2015; 211:1560–1565 [View Article][PubMed]
    [Google Scholar]
  37. Comar M, Zanotta N, Bovenzi M, Campello C. JCV/BKV and SV40 viral load in lymphoid tissues of young immunocompetent children from an area of north-east Italy. J Med Virol 2010; 82:1236–1240 [View Article][PubMed]
    [Google Scholar]
  38. Trusch F, Klein M, Finsterbusch T, Kühn J, Hofmann J et al. Seroprevalence of human polyomavirus 9 and cross-reactivity to African green monkey-derived lymphotropic polyomavirus. J Gen Virol 2012; 93:698–705 [View Article][PubMed]
    [Google Scholar]
  39. Patel NC, Vilchez RA, Killen DE, Zanwar P, Sroller V et al. Detection of polyomavirus SV40 in tonsils from immunocompetent children. J Clin Virol 2008; 43:66–72 [View Article][PubMed]
    [Google Scholar]
  40. Jafar S, Rodriguez-Barradas M, Graham DY, Butel JS. Serological evidence of SV40 infections in HIV-infected and HIV-negative adults. J Med Virol 1998; 54:276–284 [View Article][PubMed]
    [Google Scholar]
  41. Rollison DE, Helzlsouer KJ, Alberg AJ, Hoffman S, Hou J et al. Serum antibodies to JC virus, BK virus, simian virus 40, and the risk of incident adult astrocytic brain tumors. Cancer Epidemiol Biomarkers Prev 2003; 12:460–463[PubMed]
    [Google Scholar]
  42. Kjaerheim K, Røe OD, Waterboer T, Sehr P, Rizk R et al. Absence of SV40 antibodies or DNA fragments in prediagnostic mesothelioma serum samples. Int J Cancer 2007; 120:2459–2465 [View Article][PubMed]
    [Google Scholar]
  43. Allander T, Andreasson K, Gupta S, Bjerkner A, Bogdanovic G et al. Identification of a third human polyomavirus. J Virol 2007; 81:4130–4136 [View Article][PubMed]
    [Google Scholar]
  44. Gaynor AM, Nissen MD, Whiley DM, Mackay IM, Lambert SB et al. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog 2007; 3:e64 [View Article][PubMed]
    [Google Scholar]
  45. Bialasiewicz S, Whiley DM, Lambert SB, Nissen MD, Sloots TP. Detection of BK, JC, WU, or KI polyomaviruses in faecal, urine, blood, cerebrospinal fluid and respiratory samples. J Clin Virol 2009; 45:249–254 [View Article][PubMed]
    [Google Scholar]
  46. Nguyen NL, Le BM, Wang D. Serologic evidence of frequent human infection with WU and KI polyomaviruses. Emerg Infect Dis 2009; 15:1199–1205 [View Article][PubMed]
    [Google Scholar]
  47. Neske F, Prifert C, Scheiner B, Ewald M, Schubert J et al. High prevalence of antibodies against polyomavirus WU, polyomavirus KI, and human bocavirus in German blood donors. BMC Infect Dis 2010; 10:215 [View Article][PubMed]
    [Google Scholar]
  48. Kantola K, Sadeghi M, Lahtinen A, Koskenvuo M, Aaltonen LM et al. Merkel cell polyomavirus DNA in tumor-free tonsillar tissues and upper respiratory tract samples: implications for respiratory transmission and latency. J Clin Virol 2009; 45:292–295 [View Article][PubMed]
    [Google Scholar]
  49. Papa N, Zanotta N, Knowles A, Orzan E, Comar M. Detection of Malawi polyomavirus sequences in secondary lymphoid tissues from Italian healthy children: a transient site of infection. Virol J 2016; 13:97 [View Article][PubMed]
    [Google Scholar]
  50. Buck CB, Phan GQ, Raiji MT, Murphy PM, McDermott DH et al. Complete genome sequence of a tenth human polyomavirus. J Virol 2012; 86:10887 [View Article][PubMed]
    [Google Scholar]
  51. Feltkamp MC, Kazem S, van der Meijden E, Lauber C, Gorbalenya AE. From Stockholm to Malawi: recent developments in studying human polyomaviruses. J Gen Virol 2013; 94:482–496 [View Article][PubMed]
    [Google Scholar]
  52. Nicol JT, Leblond V, Arnold F, Guerra G, Mazzoni E et al. Seroprevalence of human Malawi polyomavirus. J Clin Microbiol 2014; 52:321–323 [View Article][PubMed]
    [Google Scholar]
  53. Berrios C, Jung J, Primi B, Wang M, Pedamallu C et al. Malawi polyomavirus is a prevalent human virus that interacts with known tumor suppressors. J Virol 2015; 89:857–862 [View Article][PubMed]
    [Google Scholar]
  54. Korup S, Rietscher J, Calvignac-Spencer S, Trusch F, Hofmann J et al. Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS One 2013; 8:e58021 [View Article][PubMed]
    [Google Scholar]
  55. Combes JD, Clavel C, Dalstein V, Gheit T, Clifford GM et al. Human papillomavirus detection in gargles, tonsil brushings, and frozen tissues in cancer-free patients. Oral Oncol 2018; 82:34–36 [View Article][PubMed]
    [Google Scholar]
  56. Combes JD, Dalstein V, Gheit T, Clifford GM, Tommasino M et al. Prevalence of human papillomavirus in tonsil brushings and gargles in cancer-free patients: The SPLIT study. Oral Oncol 2017; 66:52–57 [View Article][PubMed]
    [Google Scholar]
  57. Gillison ML, Broutian T, Pickard RK, Tong ZY, Xiao W et al. Prevalence of oral HPV infection in the United States, 2009-2010. JAMA 2012; 307:693–703 [View Article][PubMed]
    [Google Scholar]
  58. Schmitt M, Dondog B, Waterboer T, Pawlita M, Tommasino M et al. Abundance of multiple high-risk human papillomavirus (HPV) infections found in cervical cells analyzed by use of an ultrasensitive HPV genotyping assay. J Clin Microbiol 2010; 48:143–149 [View Article][PubMed]
    [Google Scholar]
  59. Schmitt M, Bravo IG, Snijders PJ, Gissmann L, Pawlita M et al. Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 2006; 44:504–512 [View Article][PubMed]
    [Google Scholar]
  60. Chen AA, Gheit T, Stellin M, Lupato V, Spinato G et al. Oncogenic DNA viruses found in salivary gland tumors. Oral Oncol 2017; 75:106–110 [View Article][PubMed]
    [Google Scholar]
  61. Rollison DE, Giuliano AR, Messina JL, Fenske NA, Cherpelis BS et al. Case-control study of Merkel cell polyomavirus infection and cutaneous squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2012; 21:74–81 [View Article][PubMed]
    [Google Scholar]
  62. Polesel J, Gheit T, Talamini R, Shahzad N, Lenardon O et al. Urinary human polyomavirus and papillomavirus infection and bladder cancer risk. Br J Cancer 2012; 106:222–226 [View Article][PubMed]
    [Google Scholar]
  63. Corbex M, Bouzbid S, Traverse-Glehen A, Aouras H, McKay-Chopin S 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 [View Article][PubMed]
    [Google Scholar]
  64. di Bonito P, Iaconelli M, Gheit T, Tommasino M, della Libera S et al. Detection of oncogenic viruses in water environments by a Luminex-based multiplex platform for high throughput screening of infectious agents. Water Res 2017; 123:549–555 [View Article][PubMed]
    [Google Scholar]
  65. Martelli F, Mencarini J, Rocca A, Malva ND, Bartolozzi D et al. Polyomavirus microRNA in saliva reveals persistent infectious status in the oral cavity. Virus Res 2018; 249:1–7 [View Article][PubMed]
    [Google Scholar]
  66. Comar M, Zanotta N, Rossi T, Pelos G, D'Agaro P. Secondary lymphoid tissue as an important site for WU polyomavirus infection in immunocompetent children. J Med Virol 2011; 83:1446–1450 [View Article][PubMed]
    [Google Scholar]
  67. Robaina TF, Mendes GS, Benati FJ, Pena GA, Silva RC et al. Shedding of polyomavirus in the saliva of immunocompetent individuals. J Med Virol 2013; 85:144–148 [View Article][PubMed]
    [Google Scholar]
  68. Castro T, Fink MCD, Figueiredo M, Braz-Silva PH, Pannuti CM et al. Polyomavirus BK and JC in individuals with chronic kidney failure, kidney transplantation, and healthy controls. J Clin Virol 2017; 89:5–9 [View Article][PubMed]
    [Google Scholar]
  69. Berger JR, Miller CS, Mootoor Y, Avdiushko SA, Kryscio RJ et al. JC virus detection in bodily fluids: clues to transmission. Clin Infect Dis 2006; 43:e9-12 [View Article][PubMed]
    [Google Scholar]
  70. Günel C, Kırdar S, Ömürlü İK, Ağdaş F. Detection of the Epstein-Barr virus, Human Bocavirus and novel KI and KU polyomaviruses in adenotonsillar tissues. Int J Pediatr Otorhinolaryngol 2015; 79:423–427 [View Article][PubMed]
    [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.001156
Loading
/content/journal/jgv/10.1099/jgv.0.001156
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error