Molecular epidemiology and risk factors associated with BK and JC polyomavirus urinary shedding after kidney allograft.


Journal

Journal of medical virology
ISSN: 1096-9071
Titre abrégé: J Med Virol
Pays: United States
ID NLM: 7705876

Informations de publication

Date de publication:
Jun 2024
Historique:
revised: 17 05 2024
received: 26 02 2024
accepted: 04 06 2024
medline: 14 6 2024
pubmed: 14 6 2024
entrez: 14 6 2024
Statut: ppublish

Résumé

Polyomaviruses BK (BKPyV) and JC (JCPyV), belonging to the Polyomaviridae, are responsible for human pathologies. In kidney transplant recipients, BKPyV replication can lead to irreversible nephron damage whereas JCPyV replication remains asymptomatic. Concomitant replication is rare and potential competition between the infections has been described. The aim of this retrospective case-control study was to describe the molecular epidemiology and risk factors associated with BKPyV and JCPyV replication in a cohort of kidney transplant recipients. In total, 655 urine samples from 460 patients were tested for BKPyV and JCPyV DNA. Positive samples were submitted to strain genotyping. Demographic and clinical characteristics were also compared. Isolated JCPyV and BKPyV was found in 16.5% and 23.3% of patients, respectively; co-replication was rare (3.9%). BKPyV strains Ib-2, Ib-1, and IVc-2 were the most prevalent. JCPyV strains mostly belonged to genotypes 4 and 1B. During follow-up, JCPyV shedding significantly reduced the risk of BKPyV DNAuria, with an odds ratio of 0.57 (95% confidence interval: 0.35-0.99), and was associated with better prognosis than BKPyV replication, based on the estimated glomerular filtration rate. Molecular epidemiology of BKPyV and JCPyV strains in our region was similar to previous studies. This study suggests that JCPyV is benign and appears to limit damaging BKPyV replication. JCPyV DNAuria screening could thus be a useful strategy to predict BKPyV-related outcomes.

Identifiants

pubmed: 38874263
doi: 10.1002/jmv.29742
doi:

Substances chimiques

DNA, Viral 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e29742

Informations de copyright

© 2024 The Author(s). Journal of Medical Virology published by Wiley Periodicals LLC.

Références

Moens U, Calvignac‐Spencer S, Lauber C, et al. ICTV virus taxonomy profile: polyomaviridae. J Gen Virol. 2017;98(6):1159‐1160.
Torres C. Evolution and molecular epidemiology of polyomaviruses. Infect Genet Evol. 2020;79:104150.
Zheng HY, Nishimoto Y, Chen Q, et al. Relationships between BK virus lineages and human populations. Microb Infect. 2007;9(2):204‐213.
Agostini HT, Deckhut A, Jobes DV, et al. Genotypes of JC virus in East, Central and Southwest Europe. J Gen Virol. 2001;82(5):1221‐1331.
Hirsch HH, Kardas P, Kranz D, Leboeuf C. The human JC polyomavirus (JCPyV): virological background and clinical implications. APMIS. 2013;121(8):685‐727.
Knowles WA. Discovery and epidemiology of the human polyomaviruses BK Virus (BKV) and JC virus (JCV). Adv Exp Med Biol. 2006;577:19‐45. doi:10.1007/0-387-32957-9_2
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(6):837‐846.
Helle F, Brochot E, Handala L, et al. Biology of the BKPyV: an update. Viruses. 2017;9(11):327.
Hirsch HH, Randhawa P. BK polyomavirus in solid organ transplantation. Am J Transplant. 2013;13(suppl 4):179‐188.
Hirsch HH, Randhawa PS. AST infectious diseases community of practice. BK polyomavirus in solid organ transplantation‐guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clin Transplant. 2019;33(9):e13528.
Komorniczak M, Król E, Lizakowski S, Dębska‐Ślizień A. Screening for polyomavirus viruria like early detection of human polyomavirus infection and replication: the results of a single‐center observation. Transplant Proc. 2022;54(4):989‐994.
Brochot E, Descamps V, Handala L, et al. BK polyomavirus in the urine for follow‐up of kidney transplant recipients. Clin Microbiol Infect. 2018;25(1):e1‐112.e5. https://www.clinicalmicrobiologyandinfection.com/article/S1198-743X(18)30545-7/fulltext
Randhawa P, Uhrmacher J, Pasculle W, et al. A comparative study of BK and JC virus infections in organ transplant recipients. J Med Virol. 2005;77(2):238‐243.
Agostini HT, Ryschkewitsch CF, Stoner GL. Genotype profile of human polyomavirus JC excreted in urine of immunocompetent individuals. J Clin Microbiol. 1996;34(1):159‐164.
Polo C, Pérez JL, Mielnichuck A, Fedele CG, Niubo J, Tenorio A. Prevalence and patterns of polyomavirus urinary excretion in immunocompetent adults and children. Clin Microbiol Infect. 2004;10(7):640‐644.
Drachenberg CB, Hirsch HH, Papadimitriou JC, et al. Polyomavirus BK versus JC replication and nephropathy in renal transplant recipients: a prospective evaluation. Transplantation. 2007;84(3):323‐330.
Delbue S, Ferraresso M, Ghio L, et al. A review on JC virus infection in kidney transplant recipients. J Immunol Res. 2013;2013:e926391.
Demey B, Tinez C, François C, et al. Risk factors for BK virus viremia and nephropathy after kidney transplantation:a systematic review. J Clin Virol. 2018;109:6‐12.
Keykhosravi S, Khosravi M, Shenagari M, et al. Determining host factors contributing to the reactivation of JC virus in kidney transplant recipients. Virol J. 2022;19:131.
Cheng XS, Bohl DL, Storch GA, et al. Inhibitory interactions between BK and JC virus among kidney transplant recipients. J Am Soc Nephrol. 2011;22(5):825‐831.
Taheri S, Kafilzadeh F, Shafa M, et al. Comparison of polyomavirus (BK virus and JC viruses) viruria in renal transplant recipients with and without kidney dysfunction. J Res Med Sci. 2011;16(7):916‐922.
Querido S, Weigert A, Pinto I, et al. Detection of JCV or BKV viruria and viremia after kidney transplantation is not associated with unfavorable outcomes. J Med Virol. 2023;95(5):e28800.
Boukoum H, Nahdi I, Sahtout W, Skiri H, Segondy M, Aouni M. BK and JC virus infections in healthy patients compared to kidney transplant recipients in Tunisia. Microb Pathog. 2016;97:204‐208.
Signorini L, Dolci M, Favi E, et al. Viral genomic characterization and replication pattern of human polyomaviruses in kidney transplant recipients. Viruses. 2020;12(11):1280.
Morel V, Martin E, François C, et al. A simple and reliable strategy for BK virus subtyping and subgrouping. J Clin Microbiol. 2017;55(4):1177‐1185.
Field N, Cohen T, Struelens MJ, et al. Strengthening the reporting of molecular epidemiology for infectious diseases (STROME‐ID): an extension of the STROBE statement. Lancet Infect Dis. 2014;14(4):341‐352.
Descamps V, Martin E, Morel V, Caliendo AM, et al. Comparative evaluation of three nucleic acid‐based assays for BK virus quantification. J Clin Microbiol. 2015;53(12):3822‐3827.
Ryschkewitsch C, Jensen P, Hou J, Fahle G, Fischer S, Major EO. 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. 2004;121(2):217‐221.
Rennert H, Fernandes H, Gilani Z, Sipley J. Development of a BK virus real‐time quantitative assay using the bioMérieux analyte‐specific reagents in plasma specimens. Am J Clin Path. 2015;144(6):909‐915.
Saundh BK, Baker R, Harris M, Hale A. A prospective study of renal transplant recipients reveals an absence of primary JC polyomavirus infections. J Clin Virol. 2016;77:101‐105.
Urbano PRP, Oliveira RR, Romano CM, Pannuti CS, Fink MCDS. Occurrence, genotypic characterization, and patterns of shedding of human polyomavirus JCPyV and BKPyV in urine samples of healthy individuals in São Paulo, Brazil. J Med Virol. 2016;88(1):153‐158.
Hussain I, Tasneem F, Umer M, et al. Specific and quantitative detection of human polyomaviruses BKPyV and JCPyV in the healthy Pakistani population. Virol J. 2017;14(1):86.
Zhong S, Randhawa PS, Ikegaya H, et al. Distribution patterns of BK polyomavirus (BKV) subtypes and subgroups in American, European and Asian populations suggest co‐migration of BKV and the human race. J Gen Virol. 2009;90(1):144‐152.
Schreiber PW, Kufner V, Hübel K, et al. Metagenomic virome sequencing in living donor and recipient kidney transplant pairs revealed JC polyomavirus transmission. Clin Infect Dis. 2019;69(6):987‐994.
Dolci M, Colico C, Ambrogi F, et al. Longitudinal study of human polyomaviruses viruria in kidney transplant recipients. Clin Exp Med. 2024;24(1):3.
Zou W, Imperiale MJ. Biology of polyomavirus miRNA. Front Microbiol. 2021;12:662892.
Assetta B, De Cecco M, O'Hara B, Atwood WJ. JC polyomavirus infection of primary human renal epithelial cells is controlled by a type I IFN‐Induced response. mBio. 2016;7(4). doi:10.1128/mbio.00903-16
Cubitt CL. Molecular genetics of the BK virus. Adv Exp Med Biol. 2006;577:85‐95. doi:10.1007/0-387-32957-9_6
Lindner JM, Cornacchione V, Sathe A, et al. Human memory B cells harbor diverse cross‐neutralizing antibodies against BK and JC polyomaviruses. Immunity. 2019;50(3):668‐676.e5.
Sharma MC, Zhou W, Martinez J, et al. Cross‐reactive CTL recognizing two HLA‐A*02‐restricted epitopes within the BK virus and JC virus VP1 polypeptides are frequent in immunocompetent individuals. Virology. 2006;350(1):128‐136.
Li J, Melenhorst J, Hensel N, et al. T‐cell responses to peptide fragments of the BK virus T antigen: implications for cross‐reactivity of immune response to JC virus. J Gen Virol. 2006;87(10):2951‐2960.
Husseiny MI, Anastasi B, Singer J, Lacey SF. A comparative study of Merkel cell, BK and JC polyomavirus infections in renal transplant recipients and healthy subjects. J Clin Virol. 2010;49(2):137‐140.
Helanterä I, Hirsch HH, Auvinen E, et al. High‐level JCPyV viruria after kidney transplantation—clinical and histopathological findings. J Clin Virol. 2016;85:75‐79.
Kusne S, Vilchez RA, Zanwar P, et al. Polyomavirus JC urinary shedding in kidney and liver transplant recipients associated with reduced creatinine clearance. J Infect Dis. 2012;206(6):875‐880.

Auteurs

Baptiste Demey (B)

Department of Virology, CHU Amiens-Picardie, Amiens, France.
AGIR Laboratory UR4294, Université Picardie Jules Verne, Amiens, France.

Aurélien Aubry (A)

Department of Virology, CHU Amiens-Picardie, Amiens, France.
AGIR Laboratory UR4294, Université Picardie Jules Verne, Amiens, France.

Véronique Descamps (V)

AGIR Laboratory UR4294, Université Picardie Jules Verne, Amiens, France.

Virginie Morel (V)

AGIR Laboratory UR4294, Université Picardie Jules Verne, Amiens, France.

My Hanh Hillary Le (MHH)

Department of Virology, CHU Amiens-Picardie, Amiens, France.

Claire Presne (C)

Department of Nephrology, Dialysis, and Transplantation, CHU Amiens-Picardie, Amiens, France.

François Brazier (F)

Department of Nephrology, Dialysis, and Transplantation, CHU Amiens-Picardie, Amiens, France.
MP3CV Laboratory EA7517, Jules Verne University of Picardie, Amiens, France.

François Helle (F)

AGIR Laboratory UR4294, Université Picardie Jules Verne, Amiens, France.

Etienne Brochot (E)

Department of Virology, CHU Amiens-Picardie, Amiens, France.
AGIR Laboratory UR4294, Université Picardie Jules Verne, Amiens, France.

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