Longitudinal study of human polyomaviruses viruria in kidney transplant recipients.
Immunosuppression
JCPyV and BKPyV replication
Kidney transplantation
Viruria
Journal
Clinical and experimental medicine
ISSN: 1591-9528
Titre abrégé: Clin Exp Med
Pays: Italy
ID NLM: 100973405
Informations de publication
Date de publication:
17 Jan 2024
17 Jan 2024
Historique:
received:
17
09
2023
accepted:
03
11
2023
medline:
17
1
2024
pubmed:
17
1
2024
entrez:
17
1
2024
Statut:
epublish
Résumé
Immunosuppression after kidney transplantation (KTx) exposes recipients to Human Polyomaviruses (HPyVs) infections, whose natural history is still misunderstood. Allograft biopsies, and urine from 58 donor-recipient pairs were collected before KTx (T0) and 1 (T1), 15 (T2), 30 (T3), 60 (T4), 90 (T5), 180 (T6), 270 (T7), 360 (T8), and 540 (T9) days after transplant. Specimens were tested for JC (JCPyV) and BK (BKPyV), by quantitative Real-Time PCR. The course of post-KTx HPyVs viruria, and the association between JCPyV viruria in recipients and donors, were evaluated. HPyVs were detected in 3/58 (5.2%) allograft biopsies. HPyVs viruria was present in 29/58 (50%) donors and 41/58 (70.7%) recipients. JCPyV DNA was detected in 26/58 (44.8%) donors and 25/58 recipients (43.1%), 19 of whom received kidney from JCPyV positive donor, whereas BKPyV genome was detected in 3 (5.2%) donors and 22 (37.9%) recipients. The median time of JCPyV, and BKPyV first episode of replication was 1, and 171 days post KTx, respectively. At T0, JCPyV viruria of donors was associated with increased risk of JCPyV replication post-KTx; recipients with JCPyV positive donors showed lower risk of BKPyV replication post-KTx. The results suggested that JCPyV may be transmitted by allograft, and that its replication post KTx might prevent BKPyV reactivation. Future investigation regarding correlation between chronic exposure to immunosuppressive agents and HPyVs urinary replication are warranted.
Identifiants
pubmed: 38231278
doi: 10.1007/s10238-023-01290-z
pii: 10.1007/s10238-023-01290-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3Subventions
Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca
ID : PRIN, Prot. 2017KM79NN
Organisme : Università degli Studi di Milano
ID : GSA-IDEA
Informations de copyright
© 2024. The Author(s).
Références
Levican J, Acevedo M, León O, Gaggero A, Aguayo F. Role of BK human polyomavirus in cancer. Infect Agent Cancer. 2018;13(1):1–8.
doi: 10.1186/s13027-018-0182-9
“ https://ictv.global/report/chapter/polyomaviridae/polyomaviridae .”
Feltkamp MCW, 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(PART3):482–96.
pubmed: 23255626
doi: 10.1099/vir.0.048462-0
Mbiandaa C, El-Meanawy A, Andrey S. Mechanisms of BK virus infection of renal cells and therapeutic implications. J Clin Virol. 2015;71:59–62.
doi: 10.1016/j.jcv.2015.08.003
Randhawa P, Baksh F, Aoki N, Tschirhart S, Finkelstein D. JC VIRUS INFECTION IN ALLOGRAFT KIDNEYS: Analysis by Polymerase Chain Reaction and Immunohistochemisty. Transplantation. 2001;71(9):1300–3.
pubmed: 11397966
doi: 10.1097/00007890-200105150-00020
Barbanti-Brodano G, Martini F, De Mattei M, Lazzarin L, Corallini A, Tognon M. BK and JC human polyomaviruses and simian virus 40: natural history of infection in humans, experimental oncogenicity, and association with human tumors. Adv Virus Res. 1998;50:69–99.
pubmed: 9520997
doi: 10.1016/S0065-3527(08)60806-4
Wiedinger K, Bitsaktsis C, Chang S. Reactivation of human polyomaviruses in immunocompromised states. J Neurovirol. 2013;20:1–8.
doi: 10.1007/s13365-014-0234-x
Adang L, Berger J. Progressive multifocal leukoencephalopathy. F1000Research. 2015;4:2–7.
doi: 10.12688/f1000research.7071.1
Ginevri F, Hirsch HH. Polyomavirus-associated nephropathy. Evidence-Based Nephrol Hypertens Ren Dis. 2009;2(6):277–84.
Vanichanan J, Udomkarnjananun S, Avihingsanon Y, Jutivorakool K. Common viral infections in kidney transplant recipients. Kidney Res Clin Pract. 2018;37(4):323–37.
pubmed: 30619688
pmcid: 6312768
doi: 10.23876/j.krcp.18.0063
Bofill-Mas S, Formiga-Cruz M, Clemente-Casares P, Calafell F, Girones R. Potential transmission of human polyomaviruses through the gastrointestinal tract after exposure to virions or viral DNA. J Virol. 2001;75(21):10290–9.
pubmed: 11581397
pmcid: 114603
doi: 10.1128/JVI.75.21.10290-10299.2001
Bohl D, Storch G, Ryschkewitsch M, Gaudreault-Keener C, Schnitzler M, Major E, Brennan D. Donor origin of BK virus in renal transplantation and role of HLA C7 in susceptibility to sustained BK viremia. Am J Transpl. 2005;5(9):2213–21.
doi: 10.1111/j.1600-6143.2005.01000.x
Schreiber PW, et al. Metagenomic virome sequencing in living donor and recipient kidney transplant pairs revealed jc polyomavirus transmission. Clin Infect Dis. 2019;69(6):987–94.
pubmed: 30508036
doi: 10.1093/cid/ciy1018
Kamminga S, Van Rijn AL, De Brouwer CS, Rotmans JI, Zaaijer HL, Feltkamp MCW. JC and Human polyomavirus 9 after kidney transplantation: An exploratory serological cohort study. J Clin Virol. 2021;143: 104944.
pubmed: 34450559
doi: 10.1016/j.jcv.2021.104944
Kusne S, et al. Polyomavirus JC urinary shedding in kidney and liver transplant recipients associated with reduced creatinine clearance. J Infect Dis. 2012;206(6):875–80.
pubmed: 22802433
pmcid: 3501156
doi: 10.1093/infdis/jis469
Imlay H, et al. Consensus definitions of BK polyomavirus nephropathy in renal transplant recipients for clinical trials. Clin Infect Dis. 2022;75(7):1210–6.
pubmed: 35100619
pmcid: 9525067
doi: 10.1093/cid/ciac071
L. Signorini et al., “Viral Genomic Characterization and Replication Pattern of Human Polyomaviruses in Kidney Transplant Recipients.”
Dolci M, et al. Particulate matter exposure increases JC polyomavirus replication in the human host. Environ Pollut. 2018;241:234–9.
pubmed: 29857306
doi: 10.1016/j.envpol.2018.05.044
Dolci M, Signorini L, Toumi W, Basile G, D’Alessandro S, Ferrante P, Delbue S. Human polyomaviruses genomes in clinical specimens of colon cancer patients. J Med Virol. 2021;93(11):6333–9.
pubmed: 33547809
doi: 10.1002/jmv.26851
Favi E, et al. Utility and safety of early allograft biopsy in adult deceased donor kidney transplant recipients. Clin Exp Nephrol. 2020;24(4):356–68.
pubmed: 31768863
doi: 10.1007/s10157-019-01821-7
Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. modification of diet in renal disease study group. Ann Intern Med. 1999;130(6):461–70.
pubmed: 10075613
doi: 10.7326/0003-4819-130-6-199903160-00002
Favi E, et al. Incidence, risk factors, and outcome of BK polyomavirus infection after kidney transplantation. World J Clin Cases. 2019;7(3):270.
pubmed: 30746369
pmcid: 6369392
doi: 10.12998/wjcc.v7.i3.270
Moroni G, et al. Causes of late transplant failure in cyclosporine-treated kidney allograft recipients. Clin Exp Nephrol. 2019;23(8):1076–86.
pubmed: 31016431
doi: 10.1007/s10157-019-01740-7
Salerno MP, et al. Metabolic syndrome and cardiovascular disease in kidney transplantation. Transplant Proc. 2011;43(4):1067–8.
pubmed: 21620054
doi: 10.1016/j.transproceed.2011.03.019
Piselli P, et al. Risk of de novo cancers after transplantation: results from a cohort of 7217 kidney transplant recipients, Italy 1997–2009. Eur J Cancer. 2013;49(2):336–44.
pubmed: 23062667
doi: 10.1016/j.ejca.2012.09.013
Weikert BC, Blumberg EA. Viral infection after renal transplantation: Surveillance and management. Clin J Am Soc Nephrol. 2008;3(SUPPL. 2):76–86.
doi: 10.2215/CJN.02900707
Wiedinger K, Bitsaktsis C, Sulie C. Reactivation of human polyomaviruses in immunocompromised states. J Neurovirol. 2014;20(1):1–8.
pubmed: 24481784
pmcid: 4000910
doi: 10.1007/s13365-014-0234-x
Hirsch HH, et al. European perspective on human polyomavirus infection, replication and disease in solid organ transplantation. Clin Microbiol Infect. 2014;20(Suppl 7):74–88.
pubmed: 24476010
doi: 10.1111/1469-0691.12538
Husseiny MI, Anastasi B, Jennifer S, 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):137–40.
pubmed: 20667770
pmcid: 2943003
doi: 10.1016/j.jcv.2010.06.017
Pagani E, Delbue S, Mancuso R, Borghi E, Tarantini L. Molecular analysis of JC virus genotypes circulating among the Italian healthy population. J Neurovirol. 2003;9:559–66.
pubmed: 13129770
doi: 10.1080/13550280390241269
Funahashi Y, Kato M, Fujita T, Takai S, Kimura Y, Gotoh M. Prevalence of polyomavirus positivity in urine after renal transplantation. Transplant Proc. 2014;46(2):564–6.
pubmed: 24656013
doi: 10.1016/j.transproceed.2013.09.053
Randhawa P, Uhrmacher J, Pasculle W, Vats A, Shapiro R, Eghtsead B, Weck K. A comparative study of BK and JC virus infections in organ transplant recipients. J Med Virol. 2005;77(2):238–43.
pubmed: 16121361
doi: 10.1002/jmv.20442
Pires EP, Bernardino-Vallinoto CV, Alves DM, Migone SRC, Machado LFA, Ishak MOG, Vallinoto ACR. Prevalence of infection by JC and BK polyomaviruses in kidney transplant recipients and patients with chronic renal disease. Transpl Infect Dis. 2011;13(6):633–7.
pubmed: 21414116
doi: 10.1111/j.1399-3062.2011.00614.x
Cheng XS, et al. Inhibitory interactions between BK and JC virus among kidney transplant recipients. J Am Soc Nephrol. 2011;22(5):825–31.
pubmed: 21511831
pmcid: 3269895
doi: 10.1681/ASN.2010080877
Querido S, 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.
pubmed: 37218583
doi: 10.1002/jmv.28800
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;77:101–5.
pubmed: 26923352
doi: 10.1016/j.jcv.2016.02.015
Saundh BK, Tibble S, Baker R, Sasnauskas K, Harris M, Hale A. Different patterns of BK and JC polyomavirus reactivation following renal transplantation. J Clin Pathol. 2010;63(8):714–8.
pubmed: 20702473
doi: 10.1136/jcp.2009.074864
Delbue S, et al. JC virus urinary excretion and seroprevalence in natalizumab-treated multiple sclerosis patients. Neurovirol. 2015;21(6):645–52.
doi: 10.1007/s13365-014-0268-0
Egli A, et al. Prevalence of polyomavirus BK and JC infection and replication in 400 healthy blood donors. J Infect Dis. 2009;199(6):837–46.
pubmed: 19434930
doi: 10.1086/597126
López V, et al. Prospective study of infection and nephropathy due to BK and JC polyomavirus in 76 kidney transplant recipients. Transplant Proc. 2008;40(9):2927–9.
pubmed: 19010150
doi: 10.1016/j.transproceed.2008.08.098
Matos A, Duque V, Beato S, Da Silva JP, Major E, Meliço-Silvestre A. Characterization of JC human polyomavirus infection in a Portuguese population. J Med Virol. 2010;82(3):494–504.
pubmed: 20087944
doi: 10.1002/jmv.21710
Brennan DC, et al. Incidence of BK with tacrolimus versus cyclosporine and impact of preemptive immunosuppression reduction. Am J Transplant. 2005;5(3):582–94.
pubmed: 15707414
doi: 10.1111/j.1600-6143.2005.00742.x
Krymskaya L, et al. Cross-reactivity of T lymphocytes recognizing a human cytotoxic T-lymphocyte epitope within BK and JC Virus VP1 Polypeptides A. Du Pasquier et al. J Virol. 2005;79(17):499–504.
doi: 10.1128/JVI.79.17.11170-11178.2005
Li J, 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 General Virol. 2006;87(10):2951–60.
doi: 10.1099/vir.0.82094-0
Chen Y, et al. Interplay of cellular and humoral immune responses against BK Virus in Kidney transplant recipients with polyomavirus nephropathy. J Virol. 2006;80(7):3495–505.
pubmed: 16537617
pmcid: 1440396
doi: 10.1128/JVI.80.7.3495-3505.2006
Brennan DC, Daller JA, Lake KD, Cibrik D, Del Castillo D. Rabbit Antithymocyte Globulin versus Basiliximab in Renal Transplantation. N Engl J Med. 2006;355:1967–77.
pubmed: 17093248
doi: 10.1056/NEJMoa060068
Elfadawy N, et al. CMV Viremia is associated with a decreased incidence of BKV reactivation after kidney and kidney-pancreas transplantation. Transplantation. 2013;96(12):1097–103.
pubmed: 24056621
doi: 10.1097/TP.0b013e3182a6890d
Hariharan S, McBride MA, Cherikh WS, Tolleris CB, Bresnahan BA, Johnson CP. Post-transplant renal function in the first year predicts long-term kidney transplant survival. Kidney Int. 2002;62(1):311–8.
pubmed: 12081593
doi: 10.1046/j.1523-1755.2002.00424.x
Shenagari M, Monfared A, Eghtedari H, Pourkazemi A, Hasandokht T, Khosravi M, Asharfkhani B. BK virus replication in renal transplant recipients: analysis of potential risk factors may contribute in reactivation”. J Clin Virol. 2017;96:7–11.
pubmed: 28915452
doi: 10.1016/j.jcv.2017.09.004
Munoz P, Fogeda M, Bouza E, Verde E, Palomo J, Banares R. Prevalence of BK virus replication among recipients of solid organ transplants. Clin Infect Dis. 2005;41(12):1720–5.
pubmed: 16288394
doi: 10.1086/498118