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Lyssaviruses and Other Bat Rhabdoviruses
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Lyssaviruses and Other Bat Rhabdoviruses

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (30 June 2021) | Viewed by 80455

Special Issue Editor

Dr. Laurent Dacheux

E-Mail Website
Guest Editor
Institut Pasteur, National Reference Centre for Rabies, WHO Collaborating Center for Reference and Research on Rabies, Lyssavirus Epidemiology and Neuropathology Unit, 75724 Paris, France
Interests: rabies; lyssavirus; rhabdovirus; animal reservoir; bat; epidemiology; virus diffusion; host-virus interaction; surveillance; public health; one health; control programs; zoonosis
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Lyssaviruses are the causative agent of rabies, an acute and always fatal form of encephalomyelitis affecting both humans and animals. Rabies virus is the prototype virus of the Lyssavirus genus in the family Rhabdoviridae, and the most common agent of this disease, causing nearly 59,000 human deaths per year worldwide. Acting as a zoonotic virus, its main animal reservoirs are carnivores and bats. However, at least 15 different other lyssavirus species have been identified so far, and two new tentative species were recently described. Nearly all of them were identified in bats, confirming that these animals represent the original host. Interestingly, most of them have been discovered only recently, with more than half in the past two decades, suggesting a potential emergence for some of them, associated with an increasing scientific interest for these viruses. However, the overall knowledge concerning these novel viruses, as well as for the genus Lyssavirus as a whole, remains largely unknown. Besides this genus, few other rhabdoviruses were also found in bats, mainly within the genera Vesiculovirus and Ledantevirus, but the related virology, ecology, and epidemiology data are even more scarce.

The aim of this Special Issue is therefore to contribute to filling these knowledge gaps, providing peer-reviewed reports, perspectives, reviews, or research articles focusing on the recent advances on lyssaviruses (including rabies virus) and other bat rhabdoviruses. This Special Issue encourages the submission of articles covering the following research areas, but not limited to these:

- Virus detection, virus diversity, and molecular biology.

- Interplay between virus and host cell.

- Determination of virus epidemiology, ecology, and mechanisms of diffusion in natural reservoirs or secondary hosts (animal or human).

- Development and evaluation of antiviral drugs and vaccines.

- Surveillance and control programs.

Dr. Laurent Dacheux
Guest Editor

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Viruses is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Lyssavirus
  • Rabies
  • Rhabdovirus
  • Bat
  • Reservoir
  • Emergence
  • Epidemiology
  • Evolution
  • Diversity
  • Transmission
  • Animal model
  • Cellular model
  • Molecular interaction
  • Diagnostic
  • Antiviral drugs
  • Vaccine
  • Surveillance
  • Control program

Published Papers (22 papers)

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14 pages, 2602 KiB  
Article
Evaluating the Impact of Anthropogenic Factors on the Dissemination of Contemporary Cosmopolitan, Arctic, and Arctic-like Rabies Viruses
by Andrei A. Deviatkin, Yulia A. Vakulenko, Mariia A. Dashian and Alexander N. Lukashev
Viruses 2022, 14(1), 66; https://doi.org/10.3390/v14010066 - 30 Dec 2021
Cited by 2 | Viewed by 1739
Abstract
Rabies is a globally prevalent viral zoonosis that causes 59,000 deaths per year and has important economic consequences. Most virus spread is associated with the migration of its primary hosts. Anthropogenic dissemination, mainly via the transportation of rabid dogs, shaped virus ecology a [...] Read more.
Rabies is a globally prevalent viral zoonosis that causes 59,000 deaths per year and has important economic consequences. Most virus spread is associated with the migration of its primary hosts. Anthropogenic dissemination, mainly via the transportation of rabid dogs, shaped virus ecology a few hundred years ago and is responsible for several current outbreaks. A systematic analysis of aberrant long-distance events in the steppe and Arctic-like groups of rabies virus was performed using statistical (Bayesian) phylogeography and plots of genetic vs. geographic distances. The two approaches produced similar results but had some significant differences and complemented each other. No phylogeographic analysis could be performed for the Arctic group because polar foxes transfer the virus across the whole circumpolar region at high velocity, and there was no correlation between genetic and geographic distances in this virus group. In the Arctic-like group and the steppe subgroup of the cosmopolitan group, a significant number of known sequences (15–20%) was associated with rapid long-distance transfers, which mainly occurred within Eurasia. Some of these events have been described previously, while others have not been documented. Most of the recent long-distance transfers apparently did not result in establishing the introduced virus, but a few had important implications for the phylogeographic history of rabies. Thus, human-mediated long-distance transmission of the rabies virus remains a significant threat that needs to be addressed. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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21 pages, 3258 KiB  
Article
Point Mutations in the Glycoprotein Ectodomain of Field Rabies Viruses Mediate Cell Culture Adaptation through Improved Virus Release in a Host Cell Dependent and Independent Manner
by Sabine Nitschel, Luca M. Zaeck, Madlin Potratz, Tobias Nolden, Verena te Kamp, Kati Franzke, Dirk Höper, Florian Pfaff and Stefan Finke
Viruses 2021, 13(10), 1989; https://doi.org/10.3390/v13101989 - 3 Oct 2021
Cited by 6 | Viewed by 2744
Abstract
Molecular details of field rabies virus (RABV) adaptation to cell culture replication are insufficiently understood. A better understanding of adaptation may not only reveal requirements for efficient RABV replication in cell lines, but may also provide novel insights into RABV biology and adaptation-related [...] Read more.
Molecular details of field rabies virus (RABV) adaptation to cell culture replication are insufficiently understood. A better understanding of adaptation may not only reveal requirements for efficient RABV replication in cell lines, but may also provide novel insights into RABV biology and adaptation-related loss of virulence and pathogenicity. Using two recombinant field rabies virus clones (rRABV Dog and rRABV Fox), we performed virus passages in three different cell lines to identify cell culture adaptive mutations. Ten passages were sufficient for the acquisition of adaptive mutations in the glycoprotein G and in the C-terminus of phosphoprotein P. Apart from the insertion of a glycosylation sequon via the mutation D247N in either virus, both acquired additional and cell line-specific mutations after passages on BHK (K425N) and MDCK-II (R346S or R350G) cells. As determined by virus replication kinetics, complementation, and immunofluorescence analysis, the major bottleneck in cell culture replication was the intracellular accumulation of field virus G protein, which was overcome after the acquisition of the adaptive mutations. Our data indicate that limited release of extracellular infectious virus at the plasma membrane is a defined characteristic of highly virulent field rabies viruses and we hypothesize that the observed suboptimal release of infectious virions is due to the inverse correlation of virus release and virulence in vivo. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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12 pages, 2930 KiB  
Article
Incursion of European Bat Lyssavirus 1 (EBLV-1) in Serotine Bats in the United Kingdom
by Arran J. Folly, Denise A. Marston, Megan Golding, Shweta Shukla, Rebekah Wilkie, Fabian Z. X. Lean, Alejandro Núñez, Lisa Worledge, James Aegerter, Ashley C. Banyard, Anthony R. Fooks, Nicholas Johnson and Lorraine M. McElhinney
Viruses 2021, 13(10), 1979; https://doi.org/10.3390/v13101979 - 1 Oct 2021
Cited by 3 | Viewed by 3366
Abstract
Lyssaviruses are an important genus of zoonotic viruses which cause the disease rabies. The United Kingdom is free of classical rabies (RABV). However, bat rabies due to European bat lyssavirus 2 (EBLV-2), has been detected in Daubenton’s bats (Myotis daubentonii) in [...] Read more.
Lyssaviruses are an important genus of zoonotic viruses which cause the disease rabies. The United Kingdom is free of classical rabies (RABV). However, bat rabies due to European bat lyssavirus 2 (EBLV-2), has been detected in Daubenton’s bats (Myotis daubentonii) in Great Britain since 1996, including a fatal human case in Scotland in 2002. Across Europe, European bat lyssavirus 1 (EBLV-1) is commonly associated with serotine bats (Eptesicus serotinus). Despite the presence of serotine bats across large parts of southern England, EBLV-1 had not previously been detected in this population. However, in 2018, EBLV-1 was detected through passive surveillance in a serotine bat from Dorset, England, using a combination of fluorescent antibody test, reverse transcription-PCR, Sanger sequencing and immunohistochemical analysis. Subsequent EBLV-1 positive serotine bats have been identified in South West England, again through passive surveillance, during 2018, 2019 and 2020. Here, we confirm details of seven cases of EBLV-1 and present similarities in genetic sequence indicating that emergence of EBLV-1 is likely to be recent, potentially associated with the natural movement of bats from the near continent Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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13 pages, 3367 KiB  
Communication
Glycoproteins of Predicted Amphibian and Reptile Lyssaviruses Can Mediate Infection of Mammalian and Reptile Cells
by Martina Oberhuber, Anika Schopf, Alexandru Adrian Hennrich, Rosalía Santos-Mandujano, Anna Gesine Huhn, Stefan Seitz, Christiane Riedel and Karl-Klaus Conzelmann
Viruses 2021, 13(9), 1726; https://doi.org/10.3390/v13091726 - 30 Aug 2021
Cited by 2 | Viewed by 2891
Abstract
Lyssaviruses are neurotropic rhabdoviruses thought to be restricted to mammalian hosts, and to originate from bats. The identification of lyssavirus sequences from amphibians and reptiles by metatranscriptomics thus comes as a surprise and challenges the mammalian origin of lyssaviruses. The novel sequences of [...] Read more.
Lyssaviruses are neurotropic rhabdoviruses thought to be restricted to mammalian hosts, and to originate from bats. The identification of lyssavirus sequences from amphibians and reptiles by metatranscriptomics thus comes as a surprise and challenges the mammalian origin of lyssaviruses. The novel sequences of the proposed American tree frog lyssavirus (ATFLV) and anole lizard lyssavirus (ALLV) reveal substantial phylogenetic distances from each other and from bat lyssaviruses, with ATFLV being the most distant. As virus isolation has not been successful yet, we have here studied the functionality of the authentic ATFLV- and ALLV-encoded glycoproteins in the context of rabies virus pseudotype particles. Cryogenic electron microscopy uncovered the incorporation of the plasmid-encoded G proteins in viral envelopes. Infection experiments revealed the infectivity of ATFLV and ALLV G-coated RABV pp for a broad spectrum of cell lines from humans, bats, and reptiles, demonstrating membrane fusion activities. As presumed, ATFLV and ALLV G RABV pp escaped neutralization by human rabies immune sera. The present findings support the existence of contagious lyssaviruses in poikilothermic animals, and reveal a broad cell tropism in vitro, similar to that of the rabies virus. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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21 pages, 3390 KiB  
Article
Assessing Rabies Vaccine Protection against a Novel Lyssavirus, Kotalahti Bat Lyssavirus
by Rebecca Shipley, Edward Wright, Fabian Z. X. Lean, David Selden, Daniel L. Horton, Anthony R. Fooks and Ashley C. Banyard
Viruses 2021, 13(5), 947; https://doi.org/10.3390/v13050947 - 20 May 2021
Cited by 12 | Viewed by 3652
Abstract
Rabies is a fatal encephalitis caused by an important group of viruses within the Lyssavirus genus. The prototype virus, rabies virus, is still the most commonly reported lyssavirus and causes approximately 59,000 human fatalities annually. The human and animal burden of the other [...] Read more.
Rabies is a fatal encephalitis caused by an important group of viruses within the Lyssavirus genus. The prototype virus, rabies virus, is still the most commonly reported lyssavirus and causes approximately 59,000 human fatalities annually. The human and animal burden of the other lyssavirus species is undefined. The original reports for the novel lyssavirus, Kotalahti bat lyssavirus (KBLV), were based on the detection of viral RNA alone. In this report we describe the successful generation of a live recombinant virus, cSN-KBLV; where the full-length genome clone of RABV vaccine strain, SAD-B19, was constructed with the glycoprotein of KBLV. Subsequent in vitro characterisation of cSN-KBLV is described here. In addition, the ability of a human rabies vaccine to confer protective immunity in vivo following challenge with this recombinant virus was assessed. Naïve or vaccinated mice were infected intracerebrally with a dose of 100 focus-forming units/30 µL of cSN-KBLV; all naïve mice and 8% (n = 1/12) of the vaccinated mice succumbed to the challenge, whilst 92% (n = 11/12) of the vaccinated mice survived to the end of the experiment. This report provides strong evidence for cross-neutralisation and cross-protection of cSN-KBLV using purified Vero cell rabies vaccine. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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16 pages, 1050 KiB  
Article
Rabies Prophylactic and Treatment Options: An In Vitro Study of siRNA- and Aptamer-Based Therapeutics
by Terence Peter Scott and Louis Hendrik Nel
Viruses 2021, 13(5), 881; https://doi.org/10.3390/v13050881 - 11 May 2021
Cited by 5 | Viewed by 2782
Abstract
If the goal of eliminating dog-mediated human rabies by 2030 is to be achieved, effective mass dog vaccination needs to be complemented by effective prophylaxis for individuals exposed to rabies. Aptamers and short-interfering RNAs (siRNAs) have been successful in therapeutics, but few studies [...] Read more.
If the goal of eliminating dog-mediated human rabies by 2030 is to be achieved, effective mass dog vaccination needs to be complemented by effective prophylaxis for individuals exposed to rabies. Aptamers and short-interfering RNAs (siRNAs) have been successful in therapeutics, but few studies have investigated their potential as rabies therapeutics. In this study, siRNAs and aptamers—using a novel selection method—were developed and tested against rabies virus (RABV) in a post-infection (p.i.) scenario. Multiple means of delivery were tested for siRNAs, including the use of Lipofectamine and conjugation with the developed aptamers. One siRNA (N53) resulted in an 80.13% reduction in viral RNA, while aptamer UPRET 2.03 demonstrated a 61.3% reduction when used alone at 2 h p.i. At 24 h p.i., chimera UPRET 2.03-N8 (aptamer-siRNA) resulted in a 36.5% inhibition of viral replication. To our knowledge, this is the first study using siRNAs or aptamers that (1) demonstrated significant inhibition of RABV using an aptamer, (2) tested Lipofectamine RNAi-Max as a means for delivery, and (3) produced significant RABV inhibition at 24 h p.i. This study serves as a proof-of-concept to potentially use aptamers and siRNAs as rabies immunoglobulin (RIG) replacements or therapeutic options for RABV and provides strong evidence towards their further investigation. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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10 pages, 3105 KiB  
Communication
Full-Genome Sequences and Phylogenetic Analysis of Archived Danish European Bat Lyssavirus 1 (EBLV-1) Emphasize a Higher Genetic Resolution and Spatial Segregation for Sublineage 1a
by Sten Calvelage, Conrad M. Freuling, Anthony R. Fooks, Dirk Höper, Denise A. Marston, Lorraine McElhinney, Thomas Bruun Rasmussen, Stefan Finke, Martin Beer and Thomas Müller
Viruses 2021, 13(4), 634; https://doi.org/10.3390/v13040634 - 7 Apr 2021
Cited by 4 | Viewed by 2443
Abstract
European bat lyssavirus type 1 (EBLV-1) is the causative agent for almost all reported rabies cases found in European bats. In recent years, increasing numbers of available EBLV-1 full genomes and their phylogenetic analyses helped to further elucidate the distribution and genetic characteristics [...] Read more.
European bat lyssavirus type 1 (EBLV-1) is the causative agent for almost all reported rabies cases found in European bats. In recent years, increasing numbers of available EBLV-1 full genomes and their phylogenetic analyses helped to further elucidate the distribution and genetic characteristics of EBLV-1 and its two subtypes, namely EBLV-1a and EBLV-1b. Nonetheless, the absence of full-genome sequences from regions with known detections of EBLV-1 still limit the understanding of the phylogeographic relations between viruses from different European regions. In this study, a set of 21 archived Danish EBLV-1 samples from the years 1985 to 2009 was processed for the acquisition of full-genome sequences using a high-throughput sequencing approach. Subsequent phylogenetic analysis encompassing all available EBLV-1 full genomes from databases revealed the Danish sequences belong to the EBLV-1a subtype and further highlighted the distinct, close phylogenetic relationship of Danish, Dutch and German isolates in this region. In addition, the formation of five putative groups nearly exclusively formed by Danish isolates and the overall increased resolution of the EBLV-1a branch indicate a higher genetic diversity and spatial segregation for this sublineage than was previously known. These results emphasize the importance of phylogenetic analyses of full-genome sequences of lyssaviruses for genetic geography. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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12 pages, 3059 KiB  
Article
Feline and Canine Rabies in New York State, USA
by Scott Brunt, Heather Solomon, Kathleen Brown and April Davis
Viruses 2021, 13(3), 450; https://doi.org/10.3390/v13030450 - 10 Mar 2021
Cited by 8 | Viewed by 3108
Abstract
In New York State, domestic animals are no longer considered rabies vector species, but given their ubiquity with humans, rabies cases in dogs and cats often result in multiple individuals requiring post-exposure prophylaxis. For over a decade, the New York State rabies laboratory [...] Read more.
In New York State, domestic animals are no longer considered rabies vector species, but given their ubiquity with humans, rabies cases in dogs and cats often result in multiple individuals requiring post-exposure prophylaxis. For over a decade, the New York State rabies laboratory has variant-typed these domestic animals to aid in epidemiological investigations, determine exposures, and generate demographic data. We produced a data set that outlined vaccination status, ownership, and rabies results. Our data demonstrate that a large percentage of felines submitted for rabies testing were not vaccinated or did not have a current rabies vaccination, while canines were largely vaccinated. Despite massive vaccination campaigns, free clinics, and education, these companion animals still occasionally contract rabies. Barring translocation events, we note that rabies-positive cats and dogs in New York State have exclusively contracted a raccoon variant. While the United States has made tremendous strides in reducing its rabies burden, we hope these data will encourage responsible pet ownership including rabies vaccinations to reduce unnecessary animal mortality, long quarantines, and post-exposure prophylaxis in humans. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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12 pages, 2167 KiB  
Article
Isolation and Characterization of Cross-Reactive Human Monoclonal Antibodies That Potently Neutralize Australian Bat Lyssavirus Variants and Other Phylogroup 1 Lyssaviruses
by Dawn L. Weir, Si’Ana A. Coggins, Bang K. Vu, Jessica Coertse, Lianying Yan, Ina L. Smith, Eric D. Laing, Wanda Markotter, Christopher C. Broder and Brian C. Schaefer
Viruses 2021, 13(3), 391; https://doi.org/10.3390/v13030391 - 1 Mar 2021
Cited by 6 | Viewed by 2835
Abstract
Australian bat lyssavirus (ABLV) is a rhabdovirus that circulates in four species of pteropid bats (ABLVp) and the yellow-bellied sheath-tailed bat (ABLVs) in mainland Australia. In the three confirmed human cases of ABLV, rabies illness preceded fatality. As with rabies virus (RABV), post-exposure [...] Read more.
Australian bat lyssavirus (ABLV) is a rhabdovirus that circulates in four species of pteropid bats (ABLVp) and the yellow-bellied sheath-tailed bat (ABLVs) in mainland Australia. In the three confirmed human cases of ABLV, rabies illness preceded fatality. As with rabies virus (RABV), post-exposure prophylaxis (PEP) for potential ABLV infections consists of wound cleansing, administration of the rabies vaccine and injection of rabies immunoglobulin (RIG) proximal to the wound. Despite the efficacy of PEP, the inaccessibility of human RIG (HRIG) in the developing world and the high immunogenicity of equine RIG (ERIG) has led to consideration of human monoclonal antibodies (hmAbs) as a passive immunization option that offers enhanced safety and specificity. Using a recombinant vesicular stomatitis virus (rVSV) expressing the glycoprotein (G) protein of ABLVs and phage display, we identified two hmAbs, A6 and F11, which completely neutralize ABLVs/ABLVp, and RABV at concentrations ranging from 0.39 and 6.25 µg/mL and 0.19 and 0.39 µg/mL respectively. A6 and F11 recognize overlapping epitopes in the lyssavirus G protein, effectively neutralizing phylogroup 1 lyssaviruses, while having little effect on phylogroup 2 and non-grouped diverse lyssaviruses. These results suggest that A6 and F11 could be effective therapeutic and diagnostic tools for phylogroup 1 lyssavirus infections. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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20 pages, 9620 KiB  
Article
Australian Bat Lyssavirus: Analysis of National Bat Surveillance Data from 2010 to 2016
by Rachel Iglesias, Keren Cox-Witton, Hume Field, Lee F. Skerratt and Janine Barrett
Viruses 2021, 13(2), 189; https://doi.org/10.3390/v13020189 - 27 Jan 2021
Cited by 8 | Viewed by 4567
Abstract
Australian bat lyssavirus (ABLV) was first described in 1996 and has been regularly detected in Australian bats since that time. While the virus does not cause population level impacts in bats and has minimal impacts on domestic animals, it does pose a public [...] Read more.
Australian bat lyssavirus (ABLV) was first described in 1996 and has been regularly detected in Australian bats since that time. While the virus does not cause population level impacts in bats and has minimal impacts on domestic animals, it does pose a public health risk. For this reason, bats are monitored for ABLV and a national dataset is collated and maintained by Wildlife Health Australia. The 2010–2016 dataset was analysed using logistic regression and time-series analysis to identify predictors of infection status in bats and the factors associated with human exposure to bats. In common with previous passive surveillance studies, we found that little red flying-foxes (Pteropus scapulatus) are more likely than other species to be infected with ABLV. In the four Australian mainland species of flying-fox, there are seasonal differences in infection risk that may be associated with reproductive cycles, with summer and autumn the seasons of greatest risk. The risk of human contact was also seasonal, with lower risk in winter. In line with other studies, we found that the circumstances in which the bat is encountered, such as exhibiting abnormal behaviour or being grounded, are risk factors for ABLV infection and human contact and should continue be key components of public health messaging. We also found evidence of biased recording of some types of information, which made interpretation of some findings more challenging. Strengthening of “One Health” linkages between public health and animal health services at the operational level could help overcome these biases in future, and greater harmonisation nationally would increase the value of the dataset. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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22 pages, 2787 KiB  
Article
Characterization of Novel Rhabdoviruses in Chinese Bats
by Dong-Sheng Luo, Bei Li, Xu-Rui Shen, Ren-Di Jiang, Yan Zhu, Jia Wu, Yi Fan, Hervé Bourhy, Ben Hu, Xing-Yi Ge, Zheng-Li Shi and Laurent Dacheux
Viruses 2021, 13(1), 64; https://doi.org/10.3390/v13010064 - 5 Jan 2021
Cited by 13 | Viewed by 4826
Abstract
Bats, the second largest order of mammals worldwide, harbor specific characteristics such as sustaining flight, a special immune system, unique habits, and ecological niches. In addition, they are the natural reservoirs of a variety of emerging or re-emerging zoonotic pathogens. Rhabdoviridae is one [...] Read more.
Bats, the second largest order of mammals worldwide, harbor specific characteristics such as sustaining flight, a special immune system, unique habits, and ecological niches. In addition, they are the natural reservoirs of a variety of emerging or re-emerging zoonotic pathogens. Rhabdoviridae is one of the most diverse families of RNA viruses, which consists of 20 ecologically diverse genera, infecting plants, mammals, birds, reptiles, and fish. To date, three bat-related genera are described, named Lyssavirus, Vesiculovirus, and Ledantevirus. However, the prevalence and the distribution of these bat-related rhabdoviruses remain largely unknown, especially in China. To fill this gap, we performed a large molecular retrospective study based on the real-time reverse transcription polymerase chain reaction (RT-qPCR) detection of lyssavirus in bat samples (1044 brain and 3532 saliva samples, from 63 different bat species) originating from 21 provinces of China during 2006–2018. None of them were positive for lyssavirus, but six bat brains (0.6%) of Rhinolophus bat species, originating from Hubei and Hainan provinces, were positive for vesiculoviruses or ledanteviruses. Based on complete genomes, these viruses were phylogenetically classified into three putative new species, tentatively named Yinshui bat virus (YSBV), Taiyi bat virus (TYBV), and Qiongzhong bat virus (QZBV). These results indicate the novel rhabdoviruses circulated in different Chinese bat populations. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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14 pages, 1491 KiB  
Article
Evaluation of Two Real-Time, TaqMan Reverse Transcription-PCR Assays for Detection of Rabies Virus in Circulating Variants from Argentina: Influence of Sequence Variation
by Diego A. Caraballo, María A. Lombardo, Paula Becker, María S. Sabio, Cristina Lema, Leila M. Martínez, Fernando J. Beltrán, Yu Li and Daniel M. Cisterna
Viruses 2021, 13(1), 23; https://doi.org/10.3390/v13010023 - 25 Dec 2020
Cited by 10 | Viewed by 3225
Abstract
In rabies diagnosis, it is essential to count on a rapid test to give a quick response. The combined sensitivity and robustness of the TaqMan RT-PCR assays (qRT-PCR) have made these methods a valuable alternative for rabies virus (RABV) detection. We conducted a [...] Read more.
In rabies diagnosis, it is essential to count on a rapid test to give a quick response. The combined sensitivity and robustness of the TaqMan RT-PCR assays (qRT-PCR) have made these methods a valuable alternative for rabies virus (RABV) detection. We conducted a study to compare the applicability of two widely used qRT-PCR assays targeting the nucleoprotein gene (LysGT1 assay) and leader sequences (LN34 qRT-PCR assay) of RABV genomes, in all variants circulating in Argentina. A total of 44 samples obtained from bats, dogs, cattle, and horses, that were previously tested for rabies by FAT and conventional RT-PCR, were used in the study. All variants were successfully detected by the pan-lyssavirus LN34 qRT-PCR assay. The LysGT1 assay failed to detect three bat-related variants. We further sequenced the region targeted by LysGT1 and demonstrated that the presence of three or more mismatches with respect to the primers and probe sequences precludes viral detection. We conclude that the LysGT1 assay is prone to yield variant-dependent false-negative test results, and in consequence, the LN34 assay would ensure more effective detection of RABV in Argentina. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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25 pages, 8557 KiB  
Article
Portable Rabies Virus Sequencing in Canine Rabies Endemic Countries Using the Oxford Nanopore MinION
by Crystal M. Gigante, Gowri Yale, Rene Edgar Condori, Niceta Cunha Costa, Nguyen Van Long, Phan Quang Minh, Vo Dinh Chuong, Nguyen Dang Tho, Nguyen Tat Thanh, Nguyen Xuan Thin, Nguyen Thi Hong Hanh, Gati Wambura, Frederick Ade, Oscar Mito, Veronicah Chuchu, Mathew Muturi, Athman Mwatondo, Katie Hampson, Samuel M. Thumbi, Byron G. Thomae, Victor Hugo de Paz, Sergio Meneses, Peninah Munyua, David Moran, Loren Cadena, Andrew Gibson, Ryan M. Wallace, Emily G. Pieracci and Yu Liadd Show full author list remove Hide full author list
Viruses 2020, 12(11), 1255; https://doi.org/10.3390/v12111255 - 4 Nov 2020
Cited by 21 | Viewed by 5437
Abstract
As countries with endemic canine rabies progress towards elimination by 2030, it will become necessary to employ techniques to help plan, monitor, and confirm canine rabies elimination. Sequencing can provide critical information to inform control and vaccination strategies by identifying genetically distinct virus [...] Read more.
As countries with endemic canine rabies progress towards elimination by 2030, it will become necessary to employ techniques to help plan, monitor, and confirm canine rabies elimination. Sequencing can provide critical information to inform control and vaccination strategies by identifying genetically distinct virus variants that may have different host reservoir species or geographic distributions. However, many rabies testing laboratories lack the resources or expertise for sequencing, especially in remote or rural areas where human rabies deaths are highest. We developed a low-cost, high throughput rabies virus sequencing method using the Oxford Nanopore MinION portable sequencer. A total of 259 sequences were generated from diverse rabies virus isolates in public health laboratories lacking rabies virus sequencing capacity in Guatemala, India, Kenya, and Vietnam. Phylogenetic analysis provided valuable insight into rabies virus diversity and distribution in these countries and identified a new rabies virus lineage in Kenya, the first published canine rabies virus sequence from Guatemala, evidence of rabies spread across an international border in Vietnam, and importation of a rabid dog into a state working to become rabies-free in India. Taken together, our evaluation highlights the MinION’s potential for low-cost, high volume sequencing of pathogens in locations with limited resources. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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20 pages, 4738 KiB  
Article
Genetic and Phenotypic Characterization of a Rabies Virus Strain Isolated from a Dog in Tokyo, Japan in the 1940s
by Tatsuki Takahashi, Maho Inukai, Michihito Sasaki, Madlin Potratz, Supasiri Jarusombuti, Yuji Fujii, Shoko Nishiyama, Stefan Finke, Kentaro Yamada, Hiroki Sakai, Hirofumi Sawa, Akira Nishizono, Makoto Sugiyama and Naoto Ito
Viruses 2020, 12(9), 914; https://doi.org/10.3390/v12090914 - 20 Aug 2020
Cited by 5 | Viewed by 3704
Abstract
The rabies virus strain Komatsugawa (Koma), which was isolated from a dog in Tokyo in the 1940s before eradication of rabies in Japan in 1957, is known as the only existent Japanese field strain (street strain). Although this strain potentially provides a useful [...] Read more.
The rabies virus strain Komatsugawa (Koma), which was isolated from a dog in Tokyo in the 1940s before eradication of rabies in Japan in 1957, is known as the only existent Japanese field strain (street strain). Although this strain potentially provides a useful model to study rabies pathogenesis, little is known about its genetic and phenotypic properties. Notably, this strain underwent serial passages in rodents after isolation, indicating the possibility that it may have lost biological characteristics as a street strain. In this study, to evaluate the utility of the Koma strain for studying rabies pathogenesis, we examined the genetic properties and in vitro and in vivo phenotypes. Genome-wide genetic analyses showed that, consistent with previous findings from partial sequence analyses, the Koma strain is closely related to a Russian street strain within the Arctic-related phylogenetic clade. Phenotypic examinations in vitro revealed that the Koma strain and the representative street strains are less neurotropic than the laboratory strains. Examination by using a mouse model demonstrated that the Koma strain and the street strains are more neuroinvasive than the laboratory strains. These findings indicate that the Koma strain retains phenotypes similar to those of street strains, and is therefore useful for studying rabies pathogenesis. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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Review

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12 pages, 1306 KiB  
Review
History of Rabies Incidence and Rabies Control in Serbia in Support of the Zero by 2030 Campaign to Eliminate Dog-Mediated Human Rabies
by Srđan Stankov, Dušan Lalošević and Anthony R. Fooks
Viruses 2022, 14(1), 75; https://doi.org/10.3390/v14010075 - 31 Dec 2021
Cited by 3 | Viewed by 2760
Abstract
Urban (principally canine-mediated) rabies has been a public health risk for people living in Serbia for centuries. The first legal act in urban rabies prevention in Serbia was established in 1834 by introducing high taxes for pet dog owners. Five years later in [...] Read more.
Urban (principally canine-mediated) rabies has been a public health risk for people living in Serbia for centuries. The first legal act in urban rabies prevention in Serbia was established in 1834 by introducing high taxes for pet dog owners. Five years later in 1839, the first set of literature describing rabies prevention was issued by the health department from The Serbian Ministry of Interior. An overview of cauterization of rabies wounds was presented as the principal method of rabies post exposure prophylaxis. In 1890, a human rabies vaccination was introduced in Serbia with the royal government directive which ordered patients to be treated at the Pasteur Institute in Budapest in receipt of rabies vaccination. Urban (canine) rabies was eliminated during the 1980s, but sylvatic (principally fox-mediated) rabies still prevailed. The last human rabies case was recorded in the Province of Kosovo and Metohija in 1980. Sylvatic rabies in Serbia is in the final stages of elimination by orally vaccinating foxes (Vulpes vulpes). The only published finding of a lyssavirus among Serbian bats was made in 1954 by Dr Milan Nikolić in the vicinity of Novi Sad. In 2006, a comprehensive two-year active surveillance program of lyssaviruses in bats in Serbia was undertaken. In this single study, all of the bats from Serbia tested negative for a lyssavirus. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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23 pages, 8889 KiB  
Review
On the Use of Phylogeographic Inference to Infer the Dispersal History of Rabies Virus: A Review Study
by Kanika D. Nahata, Nena Bollen, Mandev S. Gill, Maylis Layan, Hervé Bourhy, Simon Dellicour and Guy Baele
Viruses 2021, 13(8), 1628; https://doi.org/10.3390/v13081628 - 17 Aug 2021
Cited by 9 | Viewed by 4317
Abstract
Rabies is a neglected zoonotic disease which is caused by negative strand RNA-viruses belonging to the genus Lyssavirus. Within this genus, rabies viruses circulate in a diverse set of mammalian reservoir hosts, is present worldwide, and is almost always fatal in non-vaccinated [...] Read more.
Rabies is a neglected zoonotic disease which is caused by negative strand RNA-viruses belonging to the genus Lyssavirus. Within this genus, rabies viruses circulate in a diverse set of mammalian reservoir hosts, is present worldwide, and is almost always fatal in non-vaccinated humans. Approximately 59,000 people are still estimated to die from rabies each year, leading to a global initiative to work towards the goal of zero human deaths from dog-mediated rabies by 2030, requiring scientific efforts from different research fields. The past decade has seen a much increased use of phylogeographic and phylodynamic analyses to study the evolution and spread of rabies virus. We here review published studies in these research areas, making a distinction between the geographic resolution associated with the available sequence data. We pay special attention to environmental factors that these studies found to be relevant to the spread of rabies virus. Importantly, we highlight a knowledge gap in terms of applying these methods when all required data were available but not fully exploited. We conclude with an overview of recent methodological developments that have yet to be applied in phylogeographic and phylodynamic analyses of rabies virus. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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19 pages, 2944 KiB  
Review
Lagos Bat Virus, an Under-Reported Rabies-Related Lyssavirus
by Jessica Coertse, Marike Geldenhuys, Kevin le Roux and Wanda Markotter
Viruses 2021, 13(4), 576; https://doi.org/10.3390/v13040576 - 29 Mar 2021
Cited by 19 | Viewed by 3750
Abstract
Lagos bat virus (LBV), one of the 17 accepted viral species of the Lyssavirus genus, was the first rabies-related virus described in 1956. This virus is endemic to the African continent and is rarely encountered. There are currently four lineages, although the observed [...] Read more.
Lagos bat virus (LBV), one of the 17 accepted viral species of the Lyssavirus genus, was the first rabies-related virus described in 1956. This virus is endemic to the African continent and is rarely encountered. There are currently four lineages, although the observed genetic diversity exceeds existing lyssavirus species demarcation criteria. Several exposures to rabid bats infected with LBV have been reported; however, no known human cases have been reported to date. This review provides the history of LBV and summarizes previous knowledge as well as new detections. Genetic diversity, pathogenesis and prevention are re-evaluated and discussed. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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13 pages, 678 KiB  
Review
Defining New Pathways to Manage the Ongoing Emergence of Bat Rabies in Latin America
by Julio A. Benavides, William Valderrama, Sergio Recuenco, Wilson Uieda, Gerardo Suzán, Rafael Avila-Flores, Andres Velasco-Villa, Marilene Almeida, Fernanda A.G. de Andrade, Baldomero Molina-Flores, Marco Antonio Natal Vigilato, Julio Cesar Augusto Pompei, Paolo Tizzani, Jorge E. Carrera, Darcy Ibanez and Daniel G. Streicker
Viruses 2020, 12(9), 1002; https://doi.org/10.3390/v12091002 - 8 Sep 2020
Cited by 35 | Viewed by 6510
Abstract
Rabies transmitted by common vampire bats (Desmodus rotundus) has been known since the early 1900s but continues to expand geographically and in the range of species and environments affected. In this review, we present current knowledge of the epidemiology and management [...] Read more.
Rabies transmitted by common vampire bats (Desmodus rotundus) has been known since the early 1900s but continues to expand geographically and in the range of species and environments affected. In this review, we present current knowledge of the epidemiology and management of rabies in D. rotundus and argue that it can be reasonably considered an emerging public health threat. We identify knowledge gaps related to the landscape determinants of the bat reservoir, reduction in bites on humans and livestock, and social barriers to prevention. We discuss how new technologies including autonomously-spreading vaccines and reproductive suppressants targeting bats might manage both rabies and undesirable growth of D. rotundus populations. Finally, we highlight widespread under-reporting of human and animal mortality and the scarcity of studies that quantify the efficacy of control measures such as bat culling. Collaborations between researchers and managers will be crucial to implement the next generation of rabies management in Latin America. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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Other

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10 pages, 864 KiB  
Commentary
Renewed Public Health Threat from Emerging Lyssaviruses
by Anthony R. Fooks, Rebecca Shipley, Wanda Markotter, Noël Tordo, Conrad M. Freuling, Thomas Müller, Lorraine M. McElhinney, Ashley C. Banyard and Charles E. Rupprecht
Viruses 2021, 13(9), 1769; https://doi.org/10.3390/v13091769 - 4 Sep 2021
Cited by 17 | Viewed by 3130
Abstract
Pathogen discovery contributes to our knowledge of bat-borne viruses and is linked to the heightened interest globally in bats as recognised reservoirs of zoonotic agents. The transmission of lyssaviruses from bats-to-humans, domestic animals, or other wildlife species is uncommon, but interest in these [...] Read more.
Pathogen discovery contributes to our knowledge of bat-borne viruses and is linked to the heightened interest globally in bats as recognised reservoirs of zoonotic agents. The transmission of lyssaviruses from bats-to-humans, domestic animals, or other wildlife species is uncommon, but interest in these pathogens remains due to their ability to cause an acute, progressive, invariably fatal encephalitis in humans. Consequently, the detection and characterisation of bat lyssaviruses continues to expand our knowledge of their phylogroup definition, viral diversity, host species association, geographical distribution, evolution, mechanisms for perpetuation, and the potential routes of transmission. Although the opportunity for lyssavirus cross-species transmission seems rare, adaptation in a new host and the possibility of onward transmission to humans requires continued investigation. Considering the limited efficacy of available rabies biologicals it is important to further our understanding of protective immunity to minimize the threat from these pathogens to public health. Hence, in addition to increased surveillance, the development of a niche pan-lyssavirus vaccine or therapeutic biologics for post-exposure prophylaxis for use against genetically divergent lyssaviruses should be an international priority as these emerging lyssaviruses remain a concern for global public health. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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12 pages, 1273 KiB  
Brief Report
Phenotypic Divergence of P Proteins of Australian Bat Lyssavirus Lineages Circulating in Microbats and Flying Foxes
by Celine Deffrasnes, Meng-Xiao Luo, Linda Wiltzer-Bach, Cassandra T. David, Kim G. Lieu, Lin-Fa Wang, David A. Jans, Glenn A. Marsh and Gregory W. Moseley
Viruses 2021, 13(5), 831; https://doi.org/10.3390/v13050831 - 4 May 2021
Cited by 5 | Viewed by 2510
Abstract
Bats are reservoirs of many pathogenic viruses, including the lyssaviruses rabies virus (RABV) and Australian bat lyssavirus (ABLV). Lyssavirus strains are closely associated with particular host reservoir species, with evidence of specific adaptation. Associated phenotypic changes remain poorly understood but are likely to [...] Read more.
Bats are reservoirs of many pathogenic viruses, including the lyssaviruses rabies virus (RABV) and Australian bat lyssavirus (ABLV). Lyssavirus strains are closely associated with particular host reservoir species, with evidence of specific adaptation. Associated phenotypic changes remain poorly understood but are likely to involve phosphoprotein (P protein), a key mediator of the intracellular virus–host interface. Here, we examine the phenotype of P protein of ABLV, which circulates as two defined lineages associated with frugivorous and insectivorous bats, providing the opportunity to compare proteins of viruses adapted to divergent bat species. We report that key functions of P protein in the antagonism of interferon/signal transducers and activators of transcription 1 (STAT1) signaling and the capacity of P protein to undergo nuclear trafficking differ between lineages. Molecular mapping indicates that these differences are functionally distinct and appear to involve modulatory effects on regulatory regions or structural impact rather than changes to defined interaction sequences. This results in partial but significant phenotypic divergence, consistent with “fine-tuning” to host biology, and with potentially distinct properties in the virus–host interface between bat families that represent key zoonotic reservoirs. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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12 pages, 294 KiB  
Perspective
The Role of Waste Management in Control of Rabies: A Neglected Issue
by Nicolette Wright, Deepak Subedi, Saurav Pantha, Krishna Prasad Acharya and Louis Hendrik Nel
Viruses 2021, 13(2), 225; https://doi.org/10.3390/v13020225 - 1 Feb 2021
Cited by 11 | Viewed by 4540
Abstract
Despite being vaccine preventable, the global burden of dog rabies remains significant, and historically it is the rural and marginalized communities in developing countries of Africa and Asia that are most threatened by the disease. In recent years, the developing world has been [...] Read more.
Despite being vaccine preventable, the global burden of dog rabies remains significant, and historically it is the rural and marginalized communities in developing countries of Africa and Asia that are most threatened by the disease. In recent years, the developing world has been experiencing unprecedented increases in urbanization, with a correspondingly massive increase in municipal solid waste generation, among other things. Inefficient and inadequate waste collection and management, due to lack of resources and planning, led to significant increases in the volumes of waste on the streets and in open dumps, where it serves as food sources for free-roaming dogs. In this commentary, we discuss examples of poor waste management and the likely impact on rabies control efforts through the sustenance of free-roaming dogs in some dog rabies-endemic countries. We aim to stress the importance of implementing strategies that effectively address this particular issue as an important component of humane dog population management, as it relates to aspirations for the control and elimination of dog rabies per se. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
11 pages, 2653 KiB  
Brief Report
Genetic and Antigenetic Characterization of the Novel Kotalahti Bat Lyssavirus (KBLV)
by Sten Calvelage, Niina Tammiranta, Tiina Nokireki, Tuija Gadd, Elisa Eggerbauer, Luca M. Zaeck, Madlin Potratz, Claudia Wylezich, Dirk Höper, Thomas Müller, Stefan Finke and Conrad M. Freuling
Viruses 2021, 13(1), 69; https://doi.org/10.3390/v13010069 - 6 Jan 2021
Cited by 18 | Viewed by 3104
Abstract
There is a growing diversity of bat-associated lyssaviruses in the Old World. In August 2017, a dead Brandt’s bat (Myotis brandtii) tested positive for rabies and based on partial sequence analysis, the novel Kotalahti bat lyssavirus (KBLV) was identified. Because the [...] Read more.
There is a growing diversity of bat-associated lyssaviruses in the Old World. In August 2017, a dead Brandt’s bat (Myotis brandtii) tested positive for rabies and based on partial sequence analysis, the novel Kotalahti bat lyssavirus (KBLV) was identified. Because the bat was in an autolyzed state, isolation of KBLV was neither successful after three consecutive cell passages on cells nor in mice. Next generation sequencing (NGS) was applied using Ion Torrent ™ S5 technology coupled with target enrichment via hybridization-based capture (myBaits®) was used to sequence 99% of the genome, comprising of 11,878 nucleotides (nt). KBLV is most closely related to EBLV-2 (78.7% identity), followed by KHUV (79.0%) and BBLV (77.6%), supporting the assignment as phylogroup I lyssavirus. Interestingly, all of these lyssaviruses were also isolated from bat species of the genus Myotis, thus supporting that M. brandtii is likely the reservoir host. All information on antigenic and genetic divergence fulfil the species demarcation criteria by ICTV, so that we recommend KBLV as a novel species within the Lyssavirus genus. Next to sequence analyses, assignment to phylogroup I was functionally corroborated by cross-neutralization of G-deleted RABV, pseudotyped with KBLV-G by sera from RABV vaccinated humans. This suggests that conventional RABV vaccines also confer protection against the novel KBLV. Full article
(This article belongs to the Special Issue Lyssaviruses and Other Bat Rhabdoviruses)
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