#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Diagnostic options for human polyomaviruses in clinical practice


Authors: M. Saláková
Authors‘ workplace: Katedra genetiky a mikrobiologie, Přírodovědecká fakulta, Univerzita Karlova, Praha
Published in: Epidemiol. Mikrobiol. Imunol. 70, 2021, č. 3, s. 178-188
Category: Review Article

Overview

The members of the viral family Polyomavirae are widespread in the human population. According to serological studies, almost all adults are infected with at least one of this group of viruses. The primary infection usually occurs in childhood without any clinical signs, and after the primary infection, the viruses establish a persistent infection accompanied by occasional reactivation and shedding of the virus. These viruses often reactivate in immunosuppressed individuals, but only in a minority of these patients, the reactivation results in disease development. This biological property of human polyomaviruses makes laboratory diagnosis considerably difficult. The paper provides an overview of methods for diagnosing human polyomaviruses, which are commonly used for screening, and methods that are still validated by research but have the potential to improve detection and to identify patients at risk of developing diseases associated with polyomavirus infection.

Keywords:

human polyomaviruses – direct detection of polyomaviruses – indirect detection – diagnosis of selected human polyomaviruses – BK and JC polyomavirus diagnosis – MCPyV diagnosis


Sources

1. Gardner SD, Field AM, Coleman DV, Hulme B. New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet, 1971;1:1253–1257.

2. Padgett BL, Walker DL, ZuRhein GM, et al. Cultivation of papova- like virus from human brain with progressive multifocal leucoencephalopathy. Lancet, 1971;1:1257–1260.

3. Allander T, Andreasson K, Gupta S, et al. Identification of a third human polyomavirus. J Virol, 2007;81:4130–4136.

4. Gaynor AM, Nissen MD, Whiley DM, et al. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog, 2007;3:e64.

5. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science, 2008;319:1096–1100.

6. Schowalter RM, Pastrana DV, Pumphrey KA, et al. Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe, 2010;7:509–515.

7. van der Meijden E, Janssens RW, Lauber C, et al. Discovery of a new human polyomavirus associated with trichodysplasia spinulosa in an immunocompromized patient. PLoS Pathog, 2010;6:e1001024.

8. Scuda N, Hofmann J, Calvignac-Spencer S, et al. A novel human polyomavirus closely related to the african green monkey-derived lymphotropic polyomavirus. J Virol, 2011;85:4586–4590.

9. Siebrasse EA, Pastrana DV, Nguyen NL, et al. WU polyomavirus in respiratory epithelial cells from lung transplant patient with Job syndrome. Emerg Infect Dis, 2015;21:103–106.

10. Lim ES, Reyes A, Antonio M, et al. Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology, 2013;436:295–303.

11. Korup S, Rietscher J, Calvignac-Spencer S, et al. Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS One, 2013;8:e58021.

12. Mishra N, Pereira M, Rhodes RH, et al. Identification of a novel polyomavirus in a pancreatic transplant recipient with retinal blindness and vasculitic myopathy. J Infect Dis, 2014;210:1595– 1599.

13. Gheit T, Dutta S, Oliver J, et al. Isolation and characterization of a novel putative human polyomavirus. Virology, 2017;506:45– 54.

14. Calvignac-Spencer S, Feltkamp MC, Daugherty MD, et al. A taxonomy update for the family Polyomaviridae. Arch Virol, 2016;161:1739–1750.

15. Imperiale MJ, Major EO, et al. Polyomaviruses. In: Knipe DM, Howley PM, editors. Fields virology. Fifth Edition. Philadelphia: Lippincott, Williams & Wilkins; 2007. pp 2263–2298.

16. Sroller V, Hamsikova E, Ludvikova V, 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.

17. Sroller V, Hamsikova E, Ludvikova V, et al. Seroprevalence rates of BKV, JCV, and MCPyV polyomaviruses in the general Czech Republic population. J Med Virol, 2014; 86:1560–1568.

18. van der Meijden E, Bialasiewicz S, Rockett RJ, et al. Different serologic behavior of MCPyV, TSPyV, HPyV6, HPyV7 and HPyV9 polyomaviruses found on the skin. PLoS One, 2013;8:e81078.

19. Nicol JT, Robinot R, Carpentier A, 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.

20. Chesters PM, Heritage J, McCance DJ. Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues. J Infect Dis, 1983;147:676–684.

21. Salakova M, Koslabova E, Vojtechova Z, et al. Detection of human polyomaviruses MCPyV, HPyV6, and HPyV7 in malignant and non-malignant tonsillar tissues. J Med Virol, 2016;88:695– 702.

22. Sadeghi M, Wang Y, Ramqvist T, et al. Multiplex detection in tonsillar tissue of all known human polyomaviruses. BMC Infect Dis, 2017;17:409.

23. Knowles WA, Pillay D, Johnson MA, et al. Prevalence of longterm BK and JC excretion in HIV-infected adults and lack of correlation with serological markers. J Med Virol, 1999;59:474–479.

24. Schrama D, Groesser L, Ugurel S, et al. Presence of human polyomavirus 6 in mutation-specific BRAF inhibitor-induced epithelial proliferations. JAMA Dermatol, 2014;150:1180–1186.

25. Ho J, Jedrych JJ, Feng H, et al. Human polyomavirus 7-associated pruritic rash and viremia in transplant recipients. J Infect Dis, 2015;211:1560–1565.

26. Nguyen KD, Lee EE, Yue Y, et al. Human polyomavirus 6 and 7 are associated with pruritic and dyskeratotic dermatoses. J Am Acad Dermatol, 2017;76:932–940.

27. Chang Y, Moore PS. Merkel cell carcinoma: a virus-induced human cancer. Annu Rev Pathol, 2012;7:123–144.

28. Arthur RR, Dagostin S, Shah KV. Detection of BK virus and JC virus in urine and brain tissue by the polymerase chain reaction. J Clin Microbiol, 1989;27:1174–1179.

29. Salk J. Prospects for the control of AIDS by immunizing seropositive individuals. Nature, 1987;327:473–476.

30. Sueur C, Solis M, Meddeb M, et al. Toward standardization of BK virus monitoring: evaluation of the BK virus R-gene kit for quantification of BK viral load in urine, whole-blood, and plasma specimens. J Clin Microbiol, 2014;52:4298–4304.

31. Hayden RT, Sun Y, Tang L, et al. Progress in Quantitative Viral Load Testing: Variability and Impact of the WHO Quantitative International Standards. J Clin Microbiol, 2017;55:423–430.

32. Govind S, Hockley J, Morris C. Collaborative study to establish the 1st WHO international standard for BKV DNA for nucleic acid amplification technique (NAT)-based assays. WHO ECBS Report 2015: WHO/BS/2015.2270. Dostupné na www: http:// www.who.int/biologicals/expert_committee/BS2270_Establishment_ BKV_DNA_1st_WHO_IS.pdf (Accessed January 2017).

33. Govind S, Hockley J, Morris C. Collaborative study to establish the 1st WHO international standard for JCV DNA for nucleic acid amplification technique (NAT)-based assays. WHO ECBS Report 2015: WHO/BS/2015.2259. Dostupné na www: http:// www.who.int/biologicals/expert_committee/BS2259_Establishment_ JCV_DNA_1st_WHO_IS.pdf (Accessed January 2017).

34. Govind S, Hockley J, Morris C, Almond N. The development and establishment of the 1st WHO BKV International Standard for nucleic acid based techniques. Biologicals, 2019;60:75–84.

35. Bateman AC, Greninger AL, Atienza EE, et al. Quantification of BK Virus Standards by Quantitative Real-Time PCR and Droplet Digital PCR Is Confounded by Multiple Virus Populations in the WHO BKV International Standard. Clin Chem, 2017;63:761–769.

36. Greninger AL, Bateman AC, Atienza EE, et al. Copy Number Heterogeneity of JC Virus Standards. J Clin Microbiol, 2017;55:824– 831.

37. Jenkins A, Govind S, Morris C, Berry N. Complete Genome Sequence of Original Material Used To Derive the WHO International Standard for Human Polyomavirus BK DNA. Microbiol Resour Announc, 2019;8: e00911–19.

38. Berger JR, Aksamit AJ, Clifford DB, et al. PML diagnostic criteria: consensus statement from the AAN Neuroinfectious Disease Section. Neurology, 2013;80:1430–1438.

39. Giovannelli I, Ciccone N, Vaggelli G, et al. Utility of droplet digital PCR for the quantitative detection of polyomavirus JC in clinical samples. J Clin Virol, 2016;82:70–75.

40. Hanssen RC, Hansen H, Traavik T. Human endothelial cells allow passage of an archetypal BK virus (BKV) strain – a tool for cultivation and functional studies of natural BKV strains. Arch Virol, 2005;150:1449–1458.

41. Olsen GH, Hirsch HH, Rinaldo CH. Functional analysis of polyomavirus BK non-coding control region quasispecies from kidney transplant recipients. J Med Virol, 2009;81:1959–1967.

42. Knowles WA, Sasnauskas K. Comparison of cell culture-grown JC virus (primary human fetal glial cells and the JCI cell line) and recombinant JCV VP1 as antigen for the detection of anti-JCV antibody by haemagglutination inhibition. J Virol Methods, 2003;109:47–54.

43. Miyamura T, Yoshiike K, Takemoto KK. Characterization of JC papovavirus adapted to growth in human embryonic kidney cells. J Virol, 1980;35:498–504.

44. Akatani K, Imai M, Kimura M, et al. Propagation of JC virus in human neuroblastoma cell line IMR-32. J Med Virol, 1994;43:13–19.

45. Ishaq M, Stoner GL. Differential expression of mRNAs for JC virus large and small tumor antigens in brain tissues from progressive multifocal leukoencephalopathy patients with and without AIDS. Proc Natl Acad Sci U S A, 1994;91:8283–8287.

46. Schmid H, Nitschko H, Gerth J, et al. Polyomavirus DNA and RNA detection in renal allograft biopsies: results from a European multicenter study. Transplantation, 2005;80:600–604.

47. Hirsch HH. VP1 messenger RNA levels in urine for diagnosing BK virus nephropathy? Transplantation, 2003;75:2160.

48. Imperiale MJ. Polyomavirus miRNAs: the beginning. Curr Opin Virol, 2014;7:29–32.

49. Kamminga S, van der Meijden E, Feltkamp MCW, Zaaijer HL. Seroprevalence of fourteen human polyomaviruses determined in blood donors. PLoS One, 2018;13:e0206273.

50. Comoli P, Cioni M, Basso S, et al. Immunity to Polyomavirus BK Infection: Immune Monitoring to Regulate the Balance between Risk of BKV Nephropathy and Induction of Alloimmunity. Clin Dev Immunol, 2013;256923.

51. Pastrana DV, Brennan DC, Cuburu N, et al. Neutralization serotyping of BK polyomavirus infection in kidney transplant recipients. PLoS Pathog, 2012;8:e1002650.

52. Ray U, Cinque P, Gerevini S, et al. JC polyomavirus mutants escape antibody-mediated neutralization. Sci Transl Med, 2015;7:306ra151.

53. Ginevri F, Azzi A, Hirsch HH, et al. Prospective monitoring of polyomavirus BK replication and impact of pre-emptive intervention in pediatric kidney recipients. Am J Transplant, 2007;7:2727–2735.

54. Bohl DL, Brennan DC, Ryschkewitsch C, et al. BK virus antibody titers and intensity of infections after renal transplantation. J Clin Virol, 2008;43:184–189.

55. Kean JM, Rao S, Wang M, Garcea RL. Seroepidemiology of human polyomaviruses. PLoS Pathog, 2009;5:e1000363.

56. Pietrobon S, Bononi I, Mazzoni E, et al. Specific IgG Antibodies React to Mimotopes of BK Polyomavirus, a Small DNA Tumor Virus, in Healthy Adult Sera. Front Immunol, 2017;8:236.

57. Leinikki P, Lehtinen M, Hyoty H, et al. Synthetic peptides as diagnostic tools in virology. Adv Virus Res, 1993;42:149–186.

58. Hamilton RS, Gravell M, Major EO. Comparison of antibody titers determined by hemagglutination inhibition and enzyme immunoassay for JC virus and BK virus. J Clin Microbiol, 2000;38:105– 109.

59. Gupta N, Nguyen CQ, Modica RF, et al. BK viruria and viremia in children with systemic lupus erythematosus. Pediatr Rheumatol Online J, 2017;11:21.

60. Hirsch HH, Randhawa PS. BK polyomavirus in solid organ transplantation- Guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clin Transplant, 2019;33:e13528.

61. Drachenberg CB, Papadimitriou JC, Hirsch HH, et al. Histological patterns of polyomavirus nephropathy: correlation with graft outcome and viral load. Am J Transplant, 2004;4:2082–2092.

62. Hirsch HH, Randhawa P. BK polyomavirus in solid organ transplantation. Am J Transplant, 2013;13 Suppl 4:179–188.

63. Egli A, Infanti L, Dumoulin A, et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis, 2009;199:837–846.

64. Girmanova E, Brabcova I, Bandur S, et al. A prospective longitudinal study of BK virus infection in 120 Czech renal transplant recipients. J Med Virol, 2011;83:1395–1400.

65. Hirsch HH, Randhawa P. BK virus in solid organ transplant recipients. Am J Transplant, 2009;9 Suppl 4:S136–146.

66. Schachtner T, Babel N, Reinke P. Different risk factor profiles distinguish early-onset from late-onset BKV-replication. Transpl Int, 2015;28:1081–1091.

67. Imlay H, Whitaker K, Fisher CE, Limaye AP. Clinical characteristics and outcomes of late-onset BK virus nephropathy in kidney and kidney-pancreas transplant recipients. Transpl Infect Dis, 2018;20:e12928.

68. Cesaro S, Dalianis T, Hanssen RC, et al. ECIL guidelines for the prevention, diagnosis and treatment of BK polyomavirus-associated haemorrhagic cystitis in haematopoietic stem cell transplant recipients. J Antimicrob Chemother, 2018;73:12– 21.

69. Li JY, McNicholas K, Yong TY, et al. BK virus encoded microRNAs are present in blood of renal transplant recipients with BK viral nephropathy. Am J Transplant, 2014;14:1183–1190.

70. Virtanen E, Seppala H, Helantera I, et al. BK polyomavirus microRNA expression and sequence variation in polyomavirus-associated nephropathy. J Clin Virol, 2018;102:70–76.

71. Huang Y, Zeng G, Randhawa PS. Detection of BKV encoded mature MicroRNAs in kidney transplant patients: Clinical and biologic insights. J Clin Virol, 2019;119:6–10.

72. Kim MH, Lee YH, Seo JW, et al. Urinary exosomal viral microRNA as a marker of BK virus nephropathy in kidney transplant recipients. PLoS One, 2017;12:e0190068.

73. Wunderink HF, van der Meijden E, van der Blij-de Brouwer CS, et al. Pretransplantation Donor-Recipient Pair Seroreactivity Against BK Polyomavirus Predicts Viremia and Nephropathy After Kidney Transplantation. Am J Transplant, 2017;17:161– 172.

74. Binggeli S, Egli A, Schaub S, et al. Polyomavirus BK-specific cellular immune response to VP1 and large T-antigen in kidney transplant recipients. Am J Transplant, 2007;7:1131–1139.

75. Costa C, Mantovani S, Piceghello A, et al. Evaluation of polyomavirus BK cellular immune response by an ELISpot assay and relation to viral replication in kidney transplant recipients. New Microbiol, 2014;37:219–223.

76. Ahlenstiel-Grunow T, Sester M, Sester U, et al. BK Polyomavirus- specific T Cells as a Diagnostic and Prognostic Marker for BK Polyomavirus Infections After Pediatric Kidney Transplantation. Transplantation, 2020;104(11):2393–2402.

77. Dong-Si T, Richman S, Wattjes MP, et al. Outcome and survival of asymptomatic PML in natalizumab-treated MS patients. Ann Clin Transl Neurol, 2014;1:755–764.

78. Iacobaeus E, Ryschkewitsch C, Gravell M, et al. Analysis of cerebrospinal fluid and cerebrospinal fluid cells from patients with multiple sclerosis for detection of JC virus DNA. Mult Scler, 2009;15:28–35.

79. Swinnen B, Saegeman V, Beuselinck K, et al. Predictive value of JC virus PCR in cerebrospinal fluid in the diagnosis of PML. Diagn Microbiol Infect Dis, 2019;95:114859.

80. Dumoulin A, Hirsch HH. Reevaluating and optimizing polyomavirus BK and JC real-time PCR assays to detect rare sequence polymorphisms. J Clin Microbiol, 2011;49:1382–1388.

81. Yogo Y, Sugimoto C. The archetype concept and regulatory region rearrangement. In: Khalili K, Stoner GL, editors. Human polyomaviruses. Wiley-Liss; New York; 2001. pp. 127–148.

82. Gosert R, Kardas P, Major EO, Hirsch HH. Rearranged JC virus noncoding control regions found in progressive multifocal leukoencephalopathy patient samples increase virus early gene expression and replication rate. J Virol, 2010;84:10448–10456.

83. Rudick RA, O‘Connor PW, Polman CH, et al. Assessment of JC virus DNA in blood and urine from natalizumab-treated patients. Ann Neurol, 2010;68:304–310.

84. Warnke C, Adams O, Hartung HP, Kieseier BC. Assessment of JC virus DNA in blood and urine from natalizumab-treated patients. Ann Neurol, 2011;69:215–216.

85. Gorelik L, Lerner M, Bixler S, et al. Anti-JC virus antibodies: implications for PML risk stratification. Ann Neurol, 2010;68:295–303.

86. Plavina T, Berman M, Njenga M, et al. Multi-site analytical validation of an assay to detect anti-JCV antibodies in human serum and plasma. J Clin Virol, 2012;53:65–71.

87. Lee P, Plavina T, Castro A, et al. A second-generation ELISA (STRATIFY JCVTM, DxSelectaTM) for detection of JC virus antibodies in human serum and plasma to support progressive multifocal leukoencephalopathy risk stratification. J Clin Virol, 2013;57:141–146.

88. Plavina T, Subramanyam M, Bloomgren G, et al. Anti-JC virus antibody levels in serum or plasma further define risk of natalizumab- associated progressive multifocal leukoencephalopathy. Ann Neurol, 2014;76:802–812.

89. Koralnik IJ, Du Pasquier RA, Letvin NL. JC virus-specific cytotoxic T lymphocytes in individuals with progressive multifocal leukoencephalopathy. J Virol, 2001;75:3483–3487.

90. Marzocchetti A, Tompkins T, Clifford DB, et al. Determinants of survival in progressive multifocal leukoencephalopathy. Neurology, 2009;73:1551–1558.

91. White MK, Sariyer IK, Gordon J, et al. Diagnostic assays for polyomavirus JC and progressive multifocal leukoencephalopathy. Rev Med Virol, 2016;26:102–114.

92. LeBoit PE, Burg G, Weedon D, Sarasin A. Pathology and Genetics of Skin Tumours WHO Classification of Tumours, 4rd Edition, 11th volume.

93. Paulson KG, Park SY, Vandeven NA, et al. Merkel cell carcinoma: Current US incidence and projected increases based on changing demographics. J Am Acad Dermatol, 2018;78:457–463.

94. Hirsch HH, Knowles W, Dickenmann M, et al. Prospective study of polyomavirus type BK replication and nephropathy in renal- transplant recipients. N Engl J Med, 2002;347:488–496.

95. Viscount HB, Eid AJ, Espy MJ, et al. Polyomavirus polymerase chain reaction as a surrogate marker of polyomavirus-associated nephropathy. Transplantation, 2007;84:340–345.

Labels
Hygiene and epidemiology Medical virology Clinical microbiology

Article was published in

Epidemiology, Microbiology, Immunology

Issue 3

2021 Issue 3

Most read in this issue
Login
Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account

#ADS_BOTTOM_SCRIPTS#