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Usutu, West Nile and Tickborne Encephalitis Viruses

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Human Virology and Viral Diseases".

Deadline for manuscript submissions: closed (31 December 2022) | Viewed by 34898

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Dr. Daniel Cadar

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Guest Editor

Bernhard Nocht Institut fur Tropenmedizin Hamburgdisabled, Hamburg, Germany
Interests: virus metagenomics; novel viruses; arboviruses; phylogeography; virus ecology and evolution
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Yannick Simonin

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Institut de Génétique Moléculaire de Montpellier, University of Montpellier. Pathogenesis and Control of Chronic and Emerging Infections (PCCEI), 60 Rue de Navacelles, 34394 Montpellier, CEDEX 5, France
Interests: pathogenesis and diagnosis of emerging viruses especially flaviviruses and neurotropic viruses
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

In the last decade, the number of emerging Flaviviruses described worldwide has increased considerably. Among them, the recent expansion of emerging neurotropic arthropod-borne viruses such as West Nile virus (WNV), Usutu virus (USUV), and tickborne encephalitis virus (TBEV) over their natural range of distribution, especially in Europe, deserves special attention. WNV and USUV belong to the Japanese encephalitis (JEV) serocomplex and share many common features. They are transmitted and maintained in the natural cycle by mosquitoes as vectors with birds as the main amplifying hosts, while humans and horses are considered incidental or dead-end hosts. TBEV, in the TBEV serocomplex, is maintained in an enzootic cycle involving hard ticks (Ixodes ricinus in Western Europe) and rodents as the main reservoir. WNV, USUV, and TBEV are all described as neurotropic in animals and humans, causing severe neurological disorders such as encephalitis or meningitis. Expansion and endemicity increase the spatial and temporal overlap of flaviviruses, posing significant challenges for surveillance and control.

In this Special Issue, we invite colleagues to submit their original research articles and scientific reviews to assemble a collection of papers highlighting critical advancements in our understanding of all aspects of viral infection, including (but not restricted to) cellular, molecular and immunological aspects of infection, cell–virus interactions, factors responsible for virus virulence, epidemiology, transmission, vector competence, and diagnosis. Papers involving other neurotropic flaviviruses are also welcome.

Dr. Daniel Cadar
Dr. Yannick Simonin
Guest Editors

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Keywords

USUV
WNV
TBEV
neurotropism
epidemiology
pathogenesis
cell-virus interaction
flaviviruses
arboviruses

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Published Papers (12 papers)

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Editorial

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3 pages, 189 KiB

Open AccessEditorial

Usutu, West Nile, and Tick-Borne Encephalitis Viruses

by Yannick Simonin

Viruses 2022, 14(10), 2120; https://doi.org/10.3390/v14102120 - 25 Sep 2022

Cited by 2 | Viewed by 1738

Abstract

The beginning decades of the 21st century have been marked by multiple emergence and re-emergence phenomena of viral diseases [...] Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

Research

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22 pages, 3861 KiB

Open AccessArticle

Evaluation of NS4A, NS4B, NS5 and 3′UTR Genetic Determinants of WNV Lineage 1 Virulence in Birds and Mammals

by Lise Fiacre, Steeve Lowenski, Céline Bahuon, Marine Dumarest, Bénédicte Lambrecht, Maha Dridi, Emmanuel Albina, Jennifer Richardson, Stéphan Zientara, Miguel-Ángel Jiménez-Clavero, Nathalie Pardigon, Gaëlle Gonzalez and Sylvie Lecollinet

Viruses 2023, 15(5), 1094; https://doi.org/10.3390/v15051094 - 29 Apr 2023

Cited by 3 | Viewed by 2160

Abstract

West Nile virus (WNV) is amplified in an enzootic cycle involving birds as amplifying hosts. Because they do not develop high levels of viremia, humans and horses are considered to be dead-end hosts. Mosquitoes, especially from the Culex genus, are vectors responsible for transmission between hosts. Consequently, understanding WNV epidemiology and infection requires comparative and integrated analyses in bird, mammalian, and insect hosts. So far, markers of WNV virulence have mainly been determined in mammalian model organisms (essentially mice), while data in avian models are still missing. WNV Israel 1998 (IS98) is a highly virulent strain that is closely genetically related to the strain introduced into North America in 1999, NY99 (genomic sequence homology > 99%). The latter probably entered the continent at New York City, generating the most impactful WNV outbreak ever documented in wild birds, horses, and humans. In contrast, the WNV Italy 2008 strain (IT08) induced only limited mortality in birds and mammals in Europe during the summer of 2008. To test whether genetic polymorphism between IS98 and IT08 could account for differences in disease spread and burden, we generated chimeric viruses between IS98 and IT08, focusing on the 3′ end of the genome (NS4A, NS4B, NS5, and 3′UTR regions) where most of the non-synonymous mutations were detected. In vitro and in vivo comparative analyses of parental and chimeric viruses demonstrated a role for NS4A/NS4B/5′NS5 in the decreased virulence of IT08 in SPF chickens, possibly due to the NS4B-E249D mutation. Additionally, significant differences between the highly virulent strain IS98 and the other three viruses were observed in mice, implying the existence of additional molecular determinants of virulence in mammals, such as the amino acid changes NS5-V258A, NS5-N280K, NS5-A372V, and NS5-R422K. As previously shown, our work also suggests that genetic determinants of WNV virulence can be host-dependent. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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13 pages, 945 KiB

Open AccessArticle

SARS-CoV-2 and West Nile Virus Prevalence Studies in Raccoons and Raccoon Dogs from Germany

by Markus Keller, Norbert Peter, Cora M. Holicki, Anna V. Schantz, Ute Ziegler, Martin Eiden, Dorian D. Dörge, Andreas Vilcinskas, Martin H. Groschup and Sven Klimpel

Viruses 2022, 14(11), 2559; https://doi.org/10.3390/v14112559 - 19 Nov 2022

Cited by 7 | Viewed by 4601

Abstract

Unlike farm animals, wild animals are not subject to continuous health surveillance. Individual projects designed to screen wildlife populations for specific pathogens are, therefore, also of great importance for human health. In this context, the possible formation of a reservoir for highly pathogenic zoonotic pathogens is a focus of research. Two of these pathogens that have received particular attention during the last years are the novel severe acute respiratory syndrome coronavirus type 2 (SARS-CoV-2), due to its fast global spread and high impact to the human health, and, since its introduction into Germany, the flavivirus West Nile virus (WNV). Especially in combination with invasive vertebrate species (e.g., raccoons (Procyon lotor) and raccoon dogs (Nyctereutes procyonoides) in Germany), risk analysis must be done to enable health authorities to assess the potential for the establishment of new wild life reservoirs for pathogens. Therefore, samples were collected from raccoons and raccoon dogs and analyzed for the presence of SARS-CoV-2 and WNV infections in these populations. Molecular biological and serological data obtained imply that no SARS-CoV-2 nor WNV reservoir has been established in these two wild life species yet. Future investigations need to keep an eye on these invasive carnivore populations, especially since the close contact of these animals to humans, mainly in urban areas, would make animal–human transmission a challenge for human health. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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12 pages, 2234 KiB

Open AccessArticle

A Potential Role for Substance P in West Nile Virus Neuropathogenesis

by Shannon E. Ronca, Sarah M. Gunter, Rebecca Berry Kairis, Allison Lino, Jonathan Romero, Robia G. Pautler, Alan Nimmo and Kristy O. Murray

Viruses 2022, 14(9), 1961; https://doi.org/10.3390/v14091961 - 4 Sep 2022

Cited by 2 | Viewed by 1769

Abstract

Of individuals who develop West Nile neuroinvasive disease (WNND), ~10% will die and >40% will develop long-term complications. Current treatment recommendations solely focus on supportive care; therefore, we urgently need to identify novel and effective therapeutic options. We observed a correlation between substance P (SP), a key player in neuroinflammation, and its receptor Neurokinin-1 (NK1R). Our study in a wild-type BL6 mouse model found that SP is upregulated in the brain during infection, which correlated with neuroinvasion and damage to the blood–brain barrier. Blocking the SP/NK1R interaction beginning at disease onset modestly improved survival and prolonged time to death in a small pilot study. Although SP is significantly increased in the brain of untreated WNND mice when compared to mock-infected animals, levels of WNV are unchanged, indicating that SP likely does not play a role in viral replication but may mediate the immune response to infection. Additional studies are necessary to define if SP plays a mechanistic role or if it represents other mechanistic pathways. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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17 pages, 15727 KiB

Open AccessArticle

Usutu Virus Infects Human Placental Explants and Induces Congenital Defects in Mice

by Hélène Martin, Jonathan Barthelemy, Yamileth Chin, Mathilde Bergamelli, Nathalie Moinard, Géraldine Cartron, Yann Tanguy Le Gac, Cécile E. Malnou and Yannick Simonin

Viruses 2022, 14(8), 1619; https://doi.org/10.3390/v14081619 - 25 Jul 2022

Cited by 2 | Viewed by 2690

Abstract

Usutu virus (USUV) is a neurotropic mosquito-borne flavivirus that has dispersed quickly in Europe these past years. This arbovirus mainly follows an enzootic cycle involving mosquitoes and birds, but can also infect other mammals, causing notably sporadic cases in humans. Although it is mainly asymptomatic or responsible for mild clinical symptoms, USUV has been associated with neurological disorders, such as encephalitis and meningoencephalitis, highlighting the potential health threat of this virus. Among the different transmission routes described for other flaviviruses, the capacity for some of them to be transmitted vertically has been demonstrated, notably for Zika virus or West Nile virus, which are closely related to USUV. To evaluate the ability of USUV to replicate in the placenta and gain access to the fetus, we combined the use of several trophoblast model cell lines, ex vivo human placental explant cultures from first and third trimester of pregnancy, and in vivo USUV-infected pregnant mice. Our data demonstrate that human placental cells and tissues are permissive to USUV replication, and suggest that viral transmission can occur in mice during gestation. Hence, our observations suggest that USUV could be efficiently transmitted by the vertical route. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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15 pages, 2497 KiB

Open AccessArticle

Antiviral Effect of hBD-3 and LL-37 during Human Primary Keratinocyte Infection with West Nile Virus

by Céline Chessa, Charles Bodet, Clément Jousselin, Andy Larivière, Alexia Damour, Julien Garnier, Nicolas Lévêque and Magali Garcia

Viruses 2022, 14(7), 1552; https://doi.org/10.3390/v14071552 - 15 Jul 2022

Cited by 4 | Viewed by 2356

Abstract

West Nile virus (WNV) is an emerging flavivirus transmitted through mosquito bites and responsible for a wide range of clinical manifestations. Following their inoculation within the skin, flaviviruses replicate in keratinocytes of the epidermis, inducing an innate immune response including the production of antimicrobial peptides (AMPs). Among them, the cathelicidin LL-37 and the human beta-defensin (hBD)-3 are known for their antimicrobial and immunomodulatory properties. We assessed their role during WNV infection of human primary keratinocytes. LL-37 reduced the viral load in the supernatant of infected keratinocytes and of the titer of a viral inoculum incubated in the presence of the peptide, suggesting a direct antiviral effect of this AMP. Conversely, WNV replication was not inhibited by hBD-3. The two peptides then demonstrated immunomodulatory properties whether in the context of keratinocyte stimulation by poly(I:C) or infection by WNV, but not alone. This study demonstrates the immunostimulatory properties of these two skin AMPs at the initial site of WNV replication and the ability of LL-37 to directly inactivate West Nile viral infectious particles. The results provide new information on the multiple functions of these two peptides and underline the potential of AMPs as new antiviral strategies in the fight against flaviviral infections. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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21 pages, 1708 KiB

Open AccessArticle

Seroprevalence and Risk Factors for Equine West Nile Virus Infections in Eastern Germany, 2020

by Stefanie Ganzenberg, Michael Sieg, Ute Ziegler, Martin Pfeffer, Thomas W. Vahlenkamp, Uwe Hörügel, Martin H. Groschup and Katharina L. Lohmann

Viruses 2022, 14(6), 1191; https://doi.org/10.3390/v14061191 - 30 May 2022

Cited by 12 | Viewed by 2981

Abstract

West Nile virus (WNV) infections were first detected in Germany in 2018, but information about WNV seroprevalence in horses is limited. The study’s overall goal was to gather information that would help veterinarians, horse owners, and veterinary-, and public health- authorities understand the spread of WNV in Germany and direct protective measures. For this purpose, WNV seroprevalence was determined in counties with and without previously registered WNV infections in horses, and risk factors for seropositivity were estimated. The cohort consisted of privately owned horses from nine counties in Eastern Germany. A total of 940 serum samples was tested by competitive panflavivirus ELISA (cELISA), and reactive samples were further tested by WNV IgM capture ELISA and confirmed by virus neutralization test (VNT). Information about potential risk factors was recorded by questionnaire and analyzed by logistic regression. A total of 106 serum samples showed antibodies against flaviviruses by cELISA, of which six tested positive for WNV IgM. The VNT verified a WNV infection for 54 samples (50.9%), while 35 sera neutralized tick-borne encephalitis virus (33.0%), and eight sera neutralized Usutu virus (7.5%). Hence, seroprevalence for WNV infection was 5.8% on average and was significantly higher in counties with previously registered infections (p = 0.005). The risk factor analysis showed breed type (pony), housing in counties with previously registered infections, housing type (24 h turn-out), and presence of outdoor shelter as the main significant risk factors for seropositivity. In conclusion, we estimated the extent of WNV infection in the resident horse population in Eastern Germany and showed that seroprevalence was higher in counties with previously registered equine WNV infections. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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21 pages, 4832 KiB

Open AccessArticle

West Nile Virus Neuroinfection in Humans: Peripheral Biomarkers of Neuroinflammation and Neuronal Damage

by Orianne Constant, Jonathan Barthelemy, Anna Nagy, Sara Salinas and Yannick Simonin

Viruses 2022, 14(4), 756; https://doi.org/10.3390/v14040756 - 4 Apr 2022

Cited by 21 | Viewed by 3190

Abstract

Among emerging arthropod-borne viruses (arbovirus), West Nile virus (WNV) is a flavivirus that can be associated with severe neuroinvasive infections in humans. In 2018, the European WNV epidemic resulted in over 2000 cases, representing the most important arboviral epidemic in the European continent. Characterization of inflammation and neuronal biomarkers released during WNV infection, especially in the context of neuronal impairments, could provide insight into the development of predictive tools that could be beneficial for patient outcomes. We first analyzed the inflammatory signature in the serum of WNV-infected mice and found increased concentrations of several inflammatory cytokines. We next analyzed serum and cerebrospinal-fluid (CSF) samples from a cohort of patients infected by WNV between 2018 and 2019 in Hungary to quantify a large panel of inflammatory cytokines and neurological factors. We found higher levels of inflammatory cytokines (e.g., IL4, IL6, and IL10) and neuronal factors (e.g., BDNF, GFAP, MIF, TDP-43) in the sera of WNV-infected patients with neuroinvasive disease. Furthermore, the serum inflammatory profile of these patients persisted for several weeks after initial infection, potentially leading to long-term sequelae and having a deleterious effect on brain neurovasculature. This work suggests that early signs of increased serum concentrations of inflammatory cytokines and neuronal factors could be a signature underlying the development of severe neurological impairments. Biomarkers could play an important role in patient monitoring to improve care and prevent undesirable outcomes. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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Review

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27 pages, 3568 KiB

Open AccessReview

The Japanese Encephalitis Antigenic Complex Viruses: From Structure to Immunity

by Baldeep Khare and Richard J. Kuhn

Viruses 2022, 14(10), 2213; https://doi.org/10.3390/v14102213 - 8 Oct 2022

Cited by 13 | Viewed by 3521

Abstract

In the last three decades, several flaviviruses of concern that belong to different antigenic groups have expanded geographically. This has resulted in the presence of often more than one virus from a single antigenic group in some areas, while in Europe, Africa and Australia, additionally, multiple viruses belonging to the Japanese encephalitis (JE) serogroup co-circulate. Morphological heterogeneity of flaviviruses dictates antibody recognition and affects virus neutralization, which influences infection control. The latter is further impacted by sequential infections involving diverse flaviviruses co-circulating within a region and their cross-reactivity. The ensuing complex molecular virus–host interplay leads to either cross-protection or disease enhancement; however, the molecular determinants and mechanisms driving these outcomes are unclear. In this review, we provide an overview of the epidemiology of four JE serocomplex viruses, parameters affecting flaviviral heterogeneity and antibody recognition, host immune responses and the current knowledge of the cross-reactivity involving JE serocomplex flaviviruses that leads to differential clinical outcomes, which may inform future preventative and therapeutic interventions. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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20 pages, 1809 KiB

Open AccessReview

A Journey to the Central Nervous System: Routes of Flaviviral Neuroinvasion in Human Disease

by Eleanor M. Marshall, Marion P. G. Koopmans and Barry Rockx

Viruses 2022, 14(10), 2096; https://doi.org/10.3390/v14102096 - 21 Sep 2022

Cited by 11 | Viewed by 3470

Abstract

Many arboviruses, including viruses of the Flavivirus genus, are known to cause severe neurological disease in humans, often with long-lasting, debilitating sequalae in surviving patients. These emerging pathogens impact millions of people worldwide, yet still relatively little is known about the exact mechanisms by which they gain access to the human central nervous system. This review focusses on potential haematogenous and transneural routes of neuroinvasion employed by flaviviruses and identifies numerous gaps in knowledge, especially regarding lesser-studied interfaces of possible invasion such as the blood–cerebrospinal fluid barrier, and novel routes such as the gut–brain axis. The complex balance of pro-inflammatory and antiviral immune responses to viral neuroinvasion and pathology is also discussed, especially in the context of the hypothesised Trojan horse mechanism of neuroinvasion. A greater understanding of the routes and mechanisms of arboviral neuroinvasion, and how they differ between viruses, will aid in predictive assessments of the neuroinvasive potential of new and emerging arboviruses, and may provide opportunity for attenuation, development of novel intervention strategies and rational vaccine design for highly neurovirulent arboviruses. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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Other

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10 pages, 1454 KiB

Open AccessPerspective

Co-Circulation of West Nile, Usutu, and Tick-Borne Encephalitis Viruses in the Same Area: A Great Challenge for Diagnostic and Blood and Organ Safety

by Viktória Čabanová, Jana Kerlik, Peter Kirschner, Jana Rosochová, Boris Klempa, Monika Sláviková and Martina Ličková

Viruses 2023, 15(2), 366; https://doi.org/10.3390/v15020366 - 27 Jan 2023

Cited by 6 | Viewed by 2276

Abstract

Viral infections caused by viruses from the family Flaviviridae such as Zika (ZIKV), Dengue (DENV), yellow fever (YFV), tick-borne encephalitis (TBEV), West Nile (WNV), and Usutu (USUV) are some of the most challenging diseases for recognition in clinical diagnostics and epidemiological tracking thanks to their short viremia, non-specific symptoms, and high cross-reactivity observed in laboratory techniques. In Central Europe, the most relevant endemic flaviviruses are mosquito-borne WNV and USUV, and tick-borne TBEV. All three viruses have been recognised to be responsible for human neuroinvasive diseases. Moreover, they are interrupting the blood and transplantation safety processes, when the great efforts made to save a patient’s life could be defeated by acquired infection from donors. Due to the trend of changing distribution and abundance of flaviviruses and their vectors influenced by global change, the co-circulation of WNV, USUV, and TBEV can be observed in the same area. In this perspective, we discuss the problems of flavivirus diagnostics and epidemiology monitoring in Slovakia as a model area of Central Europe, where co-circulation of WNV, USUV, and TBEV in the same zone has been recently detected. This new situation presents multiple challenges not only for diagnostics or surveillance but particularly also for blood and organ safety. We conclude that the current routinely used laboratory diagnostics and donor screening applied by the European Union (EU) regulations are out of date and the novel methods which have become available in recent years, e.g., next-gene sequencing or urine screening should be implemented immediately. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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9 pages, 666 KiB

Open AccessBrief Report

Retrospective Investigation in Horses with Encephalitis Reveals Unnoticed Circulation of West Nile Virus in Brazil

by Hegger Fritsch, Felicidade Mota Pereira, Erica Azevedo Costa, Vagner Fonseca, Stephane Tosta, Joilson Xavier, Flavia Levy, Carla de Oliveira, Gabriela Menezes, Jaqueline Lima, Lenisa Santos, Luciana Silva, Vanessa Nardy, Marcela Kelly Gómez Astete, Beatriz Senra Álvares da Silva Santos, Nágila Rocha Aguiar, Maria Isabel Maldonado Coelho Guedes, Guilherme Canhestro de Faria, Ronaldo Furtini, Safira Rachel Milanez Drumond, Gabriel Muricy Cunha, Marcia São Pedro Leal Souza, Ronaldo de Jesus, Sara A. Franco Guimarães, Italo Coelho Nuno, Ian Carlos Brito de Santana, José Eduardo Ungar de Sá, George Roma Santos, Willadesmon Santos Silva, Thiago Ferreira Guedes, Emerson Luiz Lima Araújo, Rodrigo Fabiano do Carmo Said, Carlos Frederico Campelo de Albuquerque, Cassio Roberto Leonel Peterka, Alessandro Pecego Martins Romano, Rivaldo Venâncio da Cunha, Ana Maria Bispo de Filippis, Arabela Leal e Silva de Mello, Marta Giovanetti and Luiz Carlos Junior Alcantara Show full author list Hide full author list

Viruses 2022, 14(7), 1540; https://doi.org/10.3390/v14071540 - 14 Jul 2022

Cited by 1 | Viewed by 2438

Abstract

During these past years, several studies have provided serological evidence regarding the circulation of West Nile virus (WNV) in Brazil. Despite some reports, much is still unknown regarding the genomic diversity and transmission dynamics of this virus in the country. Recently, genomic monitoring activities in horses revealed the circulation of WNV in several Brazilian regions. These findings on the paucity of genomic data reinforce the need for prompt investigation of WNV infection in horses, which may precede human cases of encephalitis in Brazil. Thus, in this study, we retrospectively screened 54 suspicious WNV samples collected between 2017 and 2020 from the spinal cord and brain of horses with encephalitis and generated three new WNV genomes from the Ceará and Bahia states, located in the northeastern region of Brazil. The Bayesian reconstruction revealed that at least two independent introduction events occurred in Brazil. The first introduction event appears to be likely related to the North American outbreak, and was estimated to have occurred in March 2013.The second introduction event appears to have occurred in September 2017 and appears to be likely related to the South American outbreak. Together, our results reinforce the importance of increasing the priority of WNV genomic monitoring in equines with encephalitis in order to track the dispersion of this emerging pathogen through the country. Full article

(This article belongs to the Special Issue Usutu, West Nile and Tickborne Encephalitis Viruses)

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