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World J Transplant. Jan 18, 2022; 12(1): 1-7
Published online Jan 18, 2022. doi: 10.5500/wjt.v12.i1.1
Human pegivirus infection after transplant: Is there an impact?
Anna Mrzljak, Bojana Simunov, Ivan Balen, Zeljka Jurekovic, Tatjana Vilibic-Cavlek
Anna Mrzljak, Department of Gastroenterology and Hepatology, University Hospital Center Zagreb, School of Medicine, University of Zagreb, Zagreb 10000, Croatia
Bojana Simunov, Zeljka Jurekovic, Department of Medicine, Merkur University Hospital, Zagreb 10000, Croatia
Ivan Balen, Department of Gastroenterology and Endocrinology, General Hospital “Dr. Josip Bencevic”, Slavonski Brod 35000, Croatia
Tatjana Vilibic-Cavlek, Department of Virology, Croatian Institute of Public Health, School of Medicine, University of Zagreb, Zagreb 10000, Croatia
ORCID number: Anna Mrzljak (0000-0001-6270-2305); Bojana Simunov (0000-0002-1768-2277); Ivan Balen (0000-0002-7071-539X); Zeljka Jurekovic (0000-0003-0690-2577); Tatjana Vilibic-Cavlek (0000-0002-1877-5547).
Author contributions: Mrzljak A made contributions to the concept and design the manuscript; Mrzljak A, Simunov B, Balen I, and Vilibic-Cavlek T were involved in writing the manuscript; Jurekovic Z critically revised the manuscript; and all authors approved the final manuscript.
Supported by the Croatian Science Foundation, Emerging and Neglected Hepatotropic Viruses after Solid Organ and Hematopoietic Stem Cell Transplantation, No. IP-2020-02-7407.
Conflict-of-interest statement: The authors declare no conflict of interest for this article.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Anna Mrzljak, FEBG, PhD, Associate Professor, Department of Gastroenterology and Hepatology, University Hospital Center Zagreb, School of Medicine, University of Zagreb, Kispaticeva ulica 12, Zagreb 10000, Croatia. anna.mrzljak@gmail.com
Received: January 31, 2021
Peer-review started: January 31, 2021
First decision: October 17, 2021
Revised: October 25, 2021
Accepted: January 6, 2022
Article in press: January 6, 2022
Published online: January 18, 2022

Abstract

The microbiome's role in transplantation has received growing interest, but the role of virome remains understudied. Pegiviruses are single-stranded positive-sense RNA viruses, historically associated with liver disease, but their path-ogenicity is controversial. In the transplantation setting, pegivirus infection does not seem to have a negative impact on the outcomes of solid-organ and hematopoietic stem cell transplant recipients. However, the role of pegiviruses as proxies in immunosuppression monitoring brings novelty to the field of virome research in immunocompromised individuals. The possible immunomodulatory effect of pegivirus infections remains to be elucidated in further trials.

Key Words: Virome, Human pegivirus, Epidemiology, Solid-organ transplant, Hematopoietic stem cell transplantation

Core Tip: Pegiviruses are single-stranded positive-sense RNA viruses, historically associated with liver disease, but their pathogenicity is controversial. Pegivirus infection does not seem to have a negative impact on the outcome of solid-organ and hematopoietic stem cell transplant recipients. However, the role of pegiviruses as proxies in immunosuppression monitoring brings novelty to the field of virome research in immunocompromised individuals.



INTRODUCTION

The microbiome's role in transplantation has received growing interest, but the role of virome remains understudied. Several studies have shown that the virome changes upon immunosuppression initiation[1,2]. Most notable is the increase in the anello-viruses but also in pegiviruses.

Pegiviruses are single-stranded positive-sense RNA viruses, most closely related to hepatitis C virus (HCV) in terms of genome organization with structural genes located at the 5' genomic region and non-structural genes at the 3' end[3]. The genome encodes a polyprotein that is co- and post-translationally cleaved into individual viral proteins. Structural proteins common to all pegiviruses are the envelope glycoproteins (E1 and E2), and non-structural proteins are NS2-NS5B[4]. Pegiviruses are classified into eleven species (pegivirus A-K) within the genus Pegivirus in the Flaviviridae family. Two pegiviruses are known to infect humans, the human pegivirus (HPgV) and the HPgV-2, but their pathogenicity is limited and no clear association with any human disease has been established[5].

HPgV was discovered in 1995 from the sera of patients with hepatitis by two independent investigator groups, who named it GB virus C and hepatitis G virus (HGV), respectively. The HPgV's E2 glycoprotein, involved in the adhesion and fusion with the host cells, targets the production of anti-HPgV antibodies, which appear after the viral clearance and provide partial protection against reinfection[6]. The virus is efficiently transmitted through sexual contact and intravenous substance use, vertically from mother to child, and through exposure to infected blood and blood components[7].

Available data suggest a high prevalence of HpgV viremia (> 40%) in populations with parenteral exposure risk[8]. Although early studies indicated that the HPgV is hepatotropic, numerous subsequent studies have shown that HPgV is rarely detectable in infected individuals’ liver tissue. In addition, no evidence of a liver disease potentially linked to HPgV was observed during the follow-up of different patient categories[7].

HPgV-2 was isolated in 2015 from the plasma of HCV-infected patients with multiple blood-borne exposures in the United States[8]. A low prevalence of HPgV-2 viremia has been noted in the general population, but there is an increase in patients with HCV infection and injecting drug users co-infected with HCV[9]. Further studies indicated that HPgV-2 is a lymphotropic but not a hepatotropic virus, which may explain the lack of association with liver disease[10].

HPgVs are distributed globally, and viral RNA is present in roughly 750 million people[6], making it ubiquitous in human populations. The prevalence of HPgV viremia from cross-sectional studies of healthy blood donors in developed countries ranges between 1% and 5%. Nearly 200000 units of HPgVs-contaminated blood products are transfused each year in the United States[11]. In comparison, in developing countries, up to 20% of blood donors have an active infection[12]. Data suggest that approximately 1.5-2.5 billion people are currently infected or have evidence of prior HPgV infection[6].

Numerous studies examined the presence of HPgV in several countries. Generally, a high HPgV prevalence is observed among subjects with parenteral exposure, including those exposed to blood and blood products, those on hemodialysis, those with a history of intravenous substance use, and patients with chronic hepatitis C or human immunodeficiency virus (HIV) infection[13].

HPGV AFTER TRANSPLANTATION OF SOLID ORGANS AND NON-SOLID ORGANS

HPgVs have received much attention due to the possible beneficial immunomodulatory effects by reducing immune activation in patients with other viral diseases such as HIV infection, hepatitis B, and Ebola virus disease[14-17]. On the other hand, HPgV viremia has also been associated with the development of non-Hodgkin lymphoma (NHL). HPgV is a lymphotropic virus that may cause persistent infection in T and B lymphocytes, reduced Fas-mediated apoptosis, and impaired T cell and interleukin-2 receptor signaling[18]. HPgV infection anticipates the development of NHL by several years and resolved infection was not associated with NHL risk[19]. Pegiviruses have been studied both in hematopoietic stem cell transplantation (HSCT) and solid-organ transplant (SOT) recipients (Table 1).

Table 1 Seroprevalence and RNA prevalence studies in different transplant populations.
Type of transplant and period
Country/region
Patients (n)
RNA prevalence
Seroprevalence
Comment
Ref.
Liver transplant; 1997-2017Japan31314.1%/No significant association between HPgV infection and liver transplant outcomes; HPgV infection induced the up-regulation of ISG expression in peripheral blood mononuclear cellsIzumi et al[27], 2019
Renal transplant; 1989-1996Italy15524%17%Not associated with disease pathogenicity; Lower serum levels of HCV-RNA in HGV/HCV co-infected carriers compared to those infected with HCV onlyDe Filippi et al[34], 2001
Renal transplant; 2015-2016Brazil6136.1%/Most common genotype 2 (80.9%), followed by G3 (9.5%), G1 (4.85), and G5 (4.8%); no significant impact on patient outcomesSavassi-Ribas et al[31], 2020
Renal transplantFrance103 HCV positive RT recipients28%/HGV infection has no detrimental effect on liver enzymes or liver histology in HCV-positive patientsRostaing et al[37], 1999
Heart transplant; 1993-1998Germany51 transplant candidates2.0%; 00; 6.0%RNA persisted after transplant; anti-E2 antibodies persisted after transplantKallinowski et al[38], 2002
Post-transplant36.0% de novo/RNA persisted in 94% infected patients; No significant correlation between the number of blood transfusions and the infection; No impact on liver disease or patient outcome
Liver transplant; 1993-1998Germany72 transplant candidates11.%/RNA persisted in 88% of infected patientsKallinowski et al[38], 2002
Post-transplant36% de novo/RNA persisted in 87% of infected patients; no significant correlation between the number of blood transfusions and the infection; no impact on liver disease or patient outcome
Kidney transplant; 1997Thailand9443%/Co-circulation of HGV and HCV RNA was detected in 12 patients (13%)Raengsakulrach et al[30], 1997
Heart transplant; 1993-1996Germany24324%/HGV infections are transfusion related; not related to the use of mechanical circulatory assist devices or immunosuppressionWolff et al[36], 1996
Liver transplant; 1989-1996Germany98Pre-tx 8.2%; post-tx 44%/None of the hepatitis B, hepatitis C, or fulminant hepatitis, were HGV-RNA positive preoperatively; HGV was frequently acquired after LT but had no impact on the short- and medium-term clinical course post-LTFischer et al[23], 1999
Liver transplant; 2007-2010Iran1069.4%/Moderate prevalence of HGV infection in liver transplant recipientsEbadi et al[39], 2011
Kidney transplant; 1986-1990United States9312%/HGV infection does not adversely affect clinical outcome during early follow-upIsaacson et al[32], 1999
Liver transplant; 1989-1996Italy136Pre-tx 18.4%; post-tx 47.8%Pre-tx 26.5%Liver transplant patients are heavily exposed to HGV before and after transplantation; HGV does not induce liver disease; most infections are self-limited and induce a protective immunity (anti-E2 antibodies presence)Silini et al[40], 1998
HSCT; 1985-1996France9529.5%/Acute GVHD, chronic GVHD, or veno-occlusive disease are similar in HGV+ and HGV- recipients in early period after allogenic BMTCorbi et al[21],1997
Kidney transplant; 1997Germany22114%40%The majority of infected individuals eliminate the virus over timeStark et al[33], 1997
Kidney transplant; NATurkey6942%/Genotype 2 is the dominant type; subgroup 2a most common of the isolatesErensoy et al[41], 2002
Liver transplant; 1993-1995United Kingdom4747%/HGV does not cause significant liver disease after LTKarayiannis et al[42], 1998
Liver transplant; 1979-1990Netherlands39Pre-tx 15.4%; post-tx 43.6%/HGV infection is highly prevalent in liver transplant patients; in the absence of HBV or HCV co-infection with, no long-term negative influence on the graftHaagsma et al[24], 1997
Kidney transplant; 1997-2000India7052.9%58.6%GBV-C/HGV RNA significantly associated with ≥ 20 hemodialysis sessionsAbraham et al[29], 2003
Liver transplant; 1990-1994United States179Pre-tx 15%; post-tx 50%/HGV infection not associated with poor outcomeHoofnagle et al[26], 1997
HSCT; 2011-2017China18818.6%/HPgV is highly prevalent in HSCT patients; blood transfusions significantly increase the risk of HPgV infectionLi et al[22], 2019
HSCT; 2014-2015Switzerland4035%/HPgV is highly prevalent and persists for several monthsVu et al[20], 2019

Studies in HSCT recipients are limited. The prevalence of HPgV in HSCT patients ranges from 18.6%, as described in the study from Switzerland[20], to almost 30% in an earlier French study[21]. As in the general population, the risk of viremia rises with the number of received blood products[20,22]. No significant influence of pegiviruses on HSCT patient outcomes was found. On the other hand, no beneficial effect of pegivirus infections is currently proven; therefore, some studies warrant HPgV donor screening for blood products used in HSCT recipients until more conclusive studies are performed[22].

Early studies in SOT recipients were done mostly in liver transplant (LT) recipients, due to the presumed hepatotropic nature of the virus, all showing a high prevalence but no significant influence on patient outcomes[23-26]. The largest of the studies included in this review is the recent Japanese study on 313 LT recipients. This monocentric study showed an increased prevalence of HPgV in LT recipients compared to hepatectomy controls[27]. As in the earlier studies, there was no significant association between HPgV infection and LT outcomes. The study showed that HPgV infection induced the up-regulation of interferon-stimulated gene (ISG) expression in peripheral blood mononuclear cells[27].

HPgV is transmitted through parenteral, sexual, and perinatal routes[28]. Parenterally exposed individuals such as hemodialysis patients, therefore, have a higher risk of infection. An Indian study using univariate analysis showed that the prevalence of GB virus C/HGV RNA was significantly associated with ≥ 20 hemodialysis sessions[29]. After the transition from dialysis, the prevalence remains high in kidney transplant (KT) recipients, ranging from 12% to 47% in different countries[30-33]. A large Italian study in KT recipients (n = 155) showed an HGV RNA and anti-HGV prevalence of 24% and 17%, respectively[34]. None of the studies above, found any influence on patient outcomes, including kidney or liver function. On the other hand, the largest study in KT recipients (Germany, n = 221)[33] showed that a much higher proportion of KT recipients were exposed to HGV, than that suggested by HGV RNA detection alone. The prevalence of HGV RNA and anti-HGV in the study was 14% and 40%, respectively. Most infected individuals eliminate the virus over time. Unfortunately, the majority of other studies did not include serological analyses. Most of the studies on HPgV were done immediately after the discovery of the virus, focusing mostly on hepatic function or the function of the transplanted organ. Only the most recent study[1] tried to include other post-transplant complications in the analysis, e.g., new-onset diabetes after transplantation or nephrotoxicity in LT recipients. The study highlighted a potential use of anellovirus infection as a proxy for determining the immunological status. At the moment there is no standard way to measure total immunosuppression, besides the widely available through levels of immunosuppressant drugs. In the same study, all of the HPgV positive participants were still alive 5 years after LT, indicating a protective role of HPgV in post-transplantation survival[1].

The paucity of other SOT recipient studies probably reflects the proportionately lower number of those transplants performed. We found no studies evaluating HPgV in simultaneous pancreas-kidney transplantations or lung transplant recipients. The studies in heart transplant recipients are concordant to those in other SOT, showing no adverse outcome but a high HPgV prevalence, up to 36%[35-42].

CONCLUSION

To conclude, pegivirus infection does not seem to have a negative impact on the outcome of transplant recipients. Nevertheless, studies are limited and lacking prospective data. What remains to be elucidated is the possible immunomodulatory effect of pegivirus infections. Also, the role of pegiviruses as proxies in immunosuppression monitoring brings novelty to the field of virome research in immunocompromised individuals. The subject deserves further research and evaluation.

Footnotes

Provenance and peer review: Invited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Transplantation

Country/Territory of origin: Croatia

Peer-review report’s scientific quality classification

Grade A (Excellent): 0

Grade B (Very good): B, B

Grade C (Good): 0

Grade D (Fair): 0

Grade E (Poor): 0

P-Reviewer: Chan WYK, Zhou S S-Editor: Wang JJ L-Editor: Wang TQ P-Editor: Wang JJ

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