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1.  Bat Rabies in France: A 24-Year Retrospective Epidemiological Study 
PLoS ONE  2014;9(6):e98622.
Since bat rabies surveillance was first implemented in France in 1989, 48 autochthonous rabies cases without human contamination have been reported using routine diagnosis methods. In this retrospective study, data on bats submitted for rabies testing were analysed in order to better understand the epidemiology of EBLV-1 in bats in France and to investigate some epidemiological trends. Of the 3176 bats submitted for rabies diagnosis from 1989 to 2013, 1.96% (48/2447 analysed) were diagnosed positive. Among the twelve recognised virus species within the Lyssavirus genus, two species were isolated in France. 47 positive bats were morphologically identified as Eptesicus serotinus and were shown to be infected by both the EBLV-1a and the EBLV-1b lineages. Isolation of BBLV in Myotis nattereri was reported once in the north-east of France in 2012. The phylogenetic characterisation of all 47 French EBLV-1 isolates sampled between 1989 and 2013 and the French BBLV sample against 21 referenced partial nucleoprotein sequences confirmed the low genetic diversity of EBLV-1 despite its extensive geographical range. Statistical analysis performed on the serotine bat data collected from 1989 to 2013 showed seasonal variation of rabies occurrence with a significantly higher proportion of positive samples detected during the autumn compared to the spring and the summer period (34% of positive bats detected in autumn, 15% in summer, 13% in spring and 12% in winter). In this study, we have provided the details of the geographical distribution of EBLV-1a in the south-west of France and the north-south division of EBLV-1b with its subdivisions into three phylogenetic groups: group B1 in the north-west, group B2 in the centre and group B3 in the north-east of France.
doi:10.1371/journal.pone.0098622
PMCID: PMC4044004  PMID: 24892287
2.  Laboratory Surveillance of Rabies in Humans, Domestic Animals, and Bats in Madagascar from 2005 to 2010 
Background. Rabies virus (RABV) has circulated in Madagascar at least since the 19th century. Objectives. To assess the circulation of lyssavirus in the island from 2005 to 2010. Materials and Methods. Animal (including bats) and human samples were tested for RABV and other lyssavirus using antigen, ribonucleic acid (RNA), and antibodies detection and virus isolation. Results. Half of the 437 domestic or tame wild terrestrial mammal brains tested were found RABV antigen positive, including 54% of the 341 dogs tested. This percentage ranged from 26% to 75% across the period. Nine of the 10 suspected human cases tested were laboratory confirmed. RABV circulation was confirmed in 34 of the 38 districts sampled. No lyssavirus RNA was detected in 1983 bats specimens. Nevertheless, antibodies against Lagos bat virus were detected in the sera of 12 among 50 Eidolon dupreanum specimens sampled. Conclusion. More than a century after the introduction of the vaccine, rabies still remains endemic in Madagascar.
doi:10.4061/2011/727821
PMCID: PMC3170745  PMID: 21991442
3.  Monoclonal antibodies to Mokola virus for identification of rabies and rabies-related viruses. 
Journal of Clinical Microbiology  1988;26(12):2489-2494.
Rabies and rabies-related virus strains were studied by using a panel of monoclonal antibodies directed against either nucleocapsid proteins or cell surface antigens of Mokola virus (Mok-3). Each strain was used in parallel to infect cultured cells and mice. Then, the patterns of reactivity of the different monoclonal antibodies were determined by the immunofluorescent-antibody staining procedure. On cells, the monoclonal antibodies differentiated fixed rabies virus strains (serotype 1) from rabies-related virus strains. The seven fixed strains (CVS, PV4, PM, Flury LEP and HEP, ERA, and SAD) reacted identically. The previous serotype groupings (serotype 2, Lagos-bat virus; serotype 3, Mokola virus; serotype 4, Duvenhage virus) established with anti-rabies monoclonal antibodies were confirmed, except for that of Lagos-bat Kindia, which appeared to be related to the African subtype of the Duvenhage serotype (Duv-2). Within the Mokola (Mok-1, -2, -3, and -5 and Umhlanga) and the Lagos-bat (Lag-1 and -2, Zimbabwe, Pinetown, and Dakar) serotypes, each strain appeared to be distinct. The African subtype of the Duvenhage serotype reacted differently from the European subtype. Within the Duvenhage serotype, subtypes Duv-4, -5, and -6 and Denmark reacted identically, while subtypes Duv-1, -2, and -3 and German Democratic Republic appeared to be distinct. The monoclonal antibodies specific for the cell surface antigens were also used in neutralization tests with all the strains. Two of them neutralized the infectivity of Mokola virus.
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PMCID: PMC266931  PMID: 3068246
4.  Demonstration of antigenic variation among rabies virus isolates by using monoclonal antibodies to nucleocapsid proteins. 
Journal of Clinical Microbiology  1986;24(4):573-580.
Rabies virus isolates from terrestrial animals in six areas of the United States were examined with a panel of monoclonal antibodies to nucleocapsid proteins. Characteristic differences in immunofluorescence reactions permitted the formation of four antigenically distinct reaction groups from the 231 isolates tested. The geographic distribution of these groups corresponded well with separate rabies enzootic areas recognized by surveillance of sylvatic rabies in the United States. Distinctive reaction patterns were also identified for viral proteins from four infected bat species, and identical patterns were found in eight isolated cases of rabies in terrestrial animals. These findings suggest that monoclonal antibodies can be used to study the prevalence, distribution, and transmission of rabies among wildlife species.
PMCID: PMC268974  PMID: 2429983
5.  Antigenic variants of rabies virus in isolates from eastern, central and northern Canada. 
Street rabies virus isolated from 51 specimens from Ontario, Quebec, Manitoba and the Northwest Territories have been typed by a panel of 36 antinucleocapsid monoclonal antibodies. Three main groups were found. The first group comprised those terrestrial mammals originating in Ontario, Quebec and the Northwest Territories. The second group was found in terrestrial mammals from Manitoba. The third heterogenous group was made up of bats from Ontario.
PMCID: PMC1236146  PMID: 3893660
6.  Naturally Acquired Rabies Virus Infections in Wild-Caught Bats 
Abstract
The study of a zoonotic disease requires an understanding of the disease incidence in animal reservoirs. Rabies incidence in bats submitted to diagnostic laboratories does not accurately reflect the true incidence in wild bat populations as a bias exists for testing bats that have been in contact with humans or pets. This article details the rabies incidence in two species of bats collected from natural settings without such bias. In this study, brain smears from 0.6% and 2.5% of wild-caught and apparently healthy Tadarida brasiliensis and Eptesicus fuscus, respectively, were positive for rabies virus (RV) antigen. Conversely, 92% of the grounded T. brasiliensis were positive for RV. Serology performed on captive colony and sick bats reveal an immune response to rabies. This work illustrates the complex interplay between immunity, disease state, and the conundrum of RV maintenance in bats.
doi:10.1089/vbz.2011.0674
PMCID: PMC3249890  PMID: 21923271
Antibodies; Bats; Rabies; Viral isolation
7.  The epidemiology of bat rabies in New York State, 1988-92. 
Epidemiology and Infection  1994;113(3):501-511.
In 1993 New York and Texas each reported a human rabies case traced to a rare variant of rabies virus found in an uncommon species of bat. This study examined the epidemiology of bat rabies in New York State. Demographic, species, and animal-contact information for bats submitted for rabies testing from 1988-92 was analysed. The prevalence of rabies in 6810 bats was 4.6%. Nearly 90% of the 308 rabid bats identified to species were the common big brown bat (Eptesicus fuscus), which comprised 62% of all submissions. Only 25 submissions were silver-haired bats (Lasionycterus noctivagans), the species associated with the two 1993 human cases of rabies, and only two of these bats were positive. Rabies was most prevalent in female bats, in bats submitted because of human [corrected] contact, and in animals tested during September and October. These results highlight the unusual circumstances surrounding the recent human rabies cases in the United States. A species of bat rarely encountered by humans, and contributing little to the total rabies cases in bats, has been implicated in the majority of the indigenously acquired human rabies cases in the United States. The factors contributing to the transmission of this rare rabies variant remain unclear.
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PMCID: PMC2271321  PMID: 7995360
8.  Rabies-related viruses. 
Five viruses related to rabies occur in Africa. Two of these, Obodhiang from Sudan and kotonkan from Nigeria, were found in insects and are only distantly related to rabies virus. The other three are antigenically more closely related to rabies. Mokola virus was isolated from shrews in Nigeria, Lagos bat virus from fruit bats in Nigeria, and Duvenhage virus from brain of a man bitten by a bat in South Africa. The public health significance of the rabies-related viruses was emphasized in Zimbabwe where in 1981 a rabies-related virus became epizootic in the dog and cat population. It is postulated that the ancestral origin of rabies virus was Africa where the greatest antigenic diversity occurs and that the ancestor may have been an insect virus. Questions are raised why rabies has not evolved more rapidly in the New World, given the frequency and ease with which antigenic changes can be induced in the laboratory, and how the virus became so extensively established in New World bats.
PMCID: PMC2596466  PMID: 6758373
9.  Insights into Persistence Mechanisms of a Zoonotic Virus in Bat Colonies Using a Multispecies Metapopulation Model 
PLoS ONE  2014;9(4):e95610.
Rabies is a worldwide zoonosis resulting from Lyssavirus infection. In Europe, Eptesicus serotinus is the most frequently reported bat species infected with Lyssavirus, and thus considered to be the reservoir of European bat Lyssavirus type 1 (EBLV-1). To date, the role of other bat species in EBLV-1 epidemiology and persistence remains unknown. Here, we built an EBLV-1−transmission model based on local observations of a three-cave and four-bat species (Myotis capaccinii, Myotis myotis, Miniopterus schreibersii, Rhinolophus ferrumequinum) system in the Balearic Islands, for which a 1995–2011 serological dataset indicated the continuous presence of EBLV-1. Eptesicus serotinus was never observed in the system during the 16-year follow-up and therefore was not included in the model. We used the model to explore virus persistence mechanisms and to assess the importance of each bat species in the transmission dynamics. We found that EBLV-1 could not be sustained if transmission between M. schreibersii and other bat species was eliminated, suggesting that this species serves as a regional reservoir. Global sensitivity analysis using Sobol's method revealed that following the rate of autumn−winter infectious contacts, M. schreibersii's incubation- and immune-period durations, but not the infectious period length, were the most relevant factors driving virus persistence.
doi:10.1371/journal.pone.0095610
PMCID: PMC3995755  PMID: 24755619
10.  High Diversity of Rabies Viruses Associated with Insectivorous Bats in Argentina: Presence of Several Independent Enzootics 
Background
Rabies is a fatal infection of the central nervous system primarily transmitted by rabid animal bites. Rabies virus (RABV) circulates through two different epidemiological cycles: terrestrial and aerial, where dogs, foxes or skunks and bats, respectively, act as the most relevant reservoirs and/or vectors. It is widely accepted that insectivorous bats are not important vectors of RABV in Argentina despite the great diversity of bat species and the extensive Argentinean territory.
Methods
We studied the positivity rate of RABV detection in different areas of the country, and the antigenic and genetic diversity of 99 rabies virus (RABV) strains obtained from 14 species of insectivorous bats collected in Argentina between 1991 and 2008.
Results
Based on the analysis of bats received for RABV analysis by the National Rabies system of surveillance, the positivity rate of RABV in insectivorous bats ranged from 3.1 to 5.4%, depending on the geographic location. The findings were distributed among an extensive area of the Argentinean territory. The 99 strains of insectivorous bat-related sequences were divided into six distinct lineages associated with Tadarida brasiliensis, Myotis spp, Eptesicus spp, Histiotus montanus, Lasiurus blosseviilli and Lasiurus cinereus. Comparison with RABV sequences obtained from insectivorous bats of the Americas revealed co-circulation of similar genetic variants in several countries. Finally, inter-species transmission, mostly related with Lasiurus species, was demonstrated in 11.8% of the samples.
Conclusions
This study demonstrates the presence of several independent enzootics of rabies in insectivorous bats of Argentina. This information is relevant to identify potential areas at risk for human and animal infection.
Author Summary
In Argentina, successful vaccination and control of terrestrial rabies in the 1980s revealed the importance of the aerial route in RABV transmission. Current distribution of cases shows a predominance of rabies by hematophagous bats in the Northern regions where rabies is a major public health concern; in contrast, in Central and Southern regions where rabies is not a major public health concern, little surveillance is performed. Based on the analysis of insectivorous bats received for RABV analysis by the National Rabies system of surveillance, the positivity rate of RABV in insectivorous bats in these regions ranged from 3.1 to 5.4%. This rate is comparable to other nations such as the United States (9–10%) where insectivorous bats are an important cause of concern for RABV surveillance systems. Antigenic and genetic analysis of a wide collection of rabies strains shows the presence of multiple endemic cycles associated with six bat insectivorous species distributed among an extensive area of the Argentinean territory and several countries of the Americas. Finally, inter-species transmission, mostly related with Lasiurus species, was demonstrated in 11.8% of the samples. Increased public education about the relationship between insectivorous bats and rabies are essential to avoid human cases and potential spread to terrestrial mammals.
doi:10.1371/journal.pntd.0001635
PMCID: PMC3348165  PMID: 22590657
11.  Susceptibility and Pathogenesis of Little Brown Bats (Myotis lucifugus) to Heterologous and Homologous Rabies Viruses 
Journal of Virology  2013;87(16):9008-9015.
Rabies virus (RABV) maintenance in bats is not well understood. Big brown bats (Eptesicus fuscus), little brown bats (Myotis lucifugus), and Mexican free-tailed bats (Tadarida brasiliensis) are the most common bats species in the United States. These colonial bat species also have the most frequent contact with humans and domestic animals. However, the silver-haired bat (Lasionycteris noctivagans) RABV is associated with the majority of human rabies virus infections in the United States and Canada. This is of interest because silver-haired bats are more solitary bats with infrequent human interaction. Our goal was to determine the likelihood of a colonial bat species becoming infected with and transmitting a heterologous RABV. To ascertain the potential of heterologous RABV infection in colonial bat species, little brown bats were inoculated with a homologous RABV or one of two heterologous RABVs. Additionally, to determine if the route of exposure influenced the disease process, bats were inoculated either intramuscularly (i.m.) or subcutaneously (s.c.) with a homologous or heterologous RABV. Our results demonstrate that intramuscular inoculation results in a more rapid progression of disease onset, whereas the incubation time in bats inoculated s.c. is significantly longer. Additionally, cross protection was not consistently achieved in bats previously inoculated with a heterologous RABV following a challenge with a homologous RABV 6 months later. Finally, bats that developed rabies following s.c. inoculation were significantly more likely to shed virus in their saliva and demonstrated increased viral dissemination. In summary, bats inoculated via the s.c. route are more likely to shed virus, thus increasing the likelihood of transmission.
doi:10.1128/JVI.03554-12
PMCID: PMC3754046  PMID: 23741002
12.  Rabies: ocular pathology. 
Ocular pathology in the first European case of human bat-borne rabies is described. The patient was a 30-year-old bat scientist who seven weeks after bat bite developed neurological symptoms and died 23 days later. Rabies virus antigens were detected in brain smears. After extensive virological studies the virus turned out to be a rabies-related virus, closely resembling the Duvenhage virus isolated from bats in South Africa in 1980. By light microscopy focal chronic inflammatory infiltration of the ciliary body and of the choroid was found. PAS-positive exudate was seen in the subretinal and in the outer plexiform layers of the retina, and retinal veins showed endothelial damage and perivascular inflammation. Many of the retinal ganglion cells were destroyed. The presence of rabies-related viral antigen in the retinal ganglion cells was shown by positive cytoplasmic immunofluorescence, though electron microscopy failed to identify definite viral structures in the retina. By immunohistochemistry glial fibrillary acidic protein was observed in the Müller's cells, which are normally negative for this antigen but express it as a reactive change when the retina is damaged. Synaptophysin, a constituent of presynaptic vesicles of normal retinal neurons, was not detected in the retina.
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PMCID: PMC1041645  PMID: 2920157
13.  Screening of Active Lyssavirus Infection in Wild Bat Populations by Viral RNA Detection on Oropharyngeal Swabs 
Journal of Clinical Microbiology  2001;39(10):3678-3683.
Brain analysis cannot be used for the investigation of active lyssavirus infection in healthy bats because most bat species are protected by conservation directives. Consequently, serology remains the only tool for performing virological studies on natural bat populations; however, the presence of antibodies merely reflects past exposure to the virus and is not a valid marker of active infection. This work describes a new nested reverse transcription (RT)-PCR technique specifically designed for the detection of the European bat virus 1 on oropharyngeal swabs obtained from bats but also able to amplify RNA from the remaining rabies-related lyssaviruses in brain samples. The technique was successfully used for surveillance of a serotine bat (Eptesicus serotinus) colony involved in a case of human exposure, in which 15 out of 71 oropharyngeal swabs were positive. Lyssavirus infection was detected on 13 oropharyngeal swabs but in only 5 brains out of the 34 animals from which simultaneous brain and oropharyngeal samples had been taken. The lyssavirus involved could be rapidly identified by automatic sequencing of the RT-PCR products obtained from 14 brains and three bat oropharyngeal swabs. In conclusion, RT-PCR using oropharyngeal swabs will permit screening of wild bat populations for active lyssavirus infection, for research or epidemiological purposes, in line not only with conservation policies but also in a more efficient manner than classical detection techniques used on the brain.
doi:10.1128/JCM.39.10.3678-3683.2001
PMCID: PMC88406  PMID: 11574590
14.  Enzootic and Epizootic Rabies Associated with Vampire Bats, Peru 
Emerging Infectious Diseases  2013;19(9):1463-1469.
During the past decade, incidence of human infection with rabies virus (RABV) spread by the common vampire bat (Desmodus rotundus) increased considerably in South America, especially in remote areas of the Amazon rainforest, where these bats commonly feed on humans. To better understand the epizootiology of rabies associated with vampire bats, we used complete sequences of the nucleoprotein gene to infer phylogenetic relationships among 157 RABV isolates collected from humans, domestic animals, and wildlife, including bats, in Peru during 2002–2007. This analysis revealed distinct geographic structuring that indicates that RABVs spread gradually and involve different vampire bat subpopulations with different transmission cycles. Three putative new RABV lineages were found in 3 non–vampire bat species that may represent new virus reservoirs. Detection of novel RABV variants and accurate identification of reservoir hosts are critically important for the prevention and control of potential virus transmission, especially to humans.
doi:10.3201/eid1909.130083
PMCID: PMC3810916
rabies; molecular epidemiology; bats; Peru; viruses; zoonoses; vampire bats
15.  Rabies Virus Infection in Eptesicus fuscus Bats Born in Captivity (Naïve Bats) 
PLoS ONE  2013;8(5):e64808.
The study of rabies virus infection in bats can be challenging due to quarantine requirements, husbandry concerns, genetic differences among animals, and lack of medical history. To date, all rabies virus (RABV) studies in bats have been performed in wild caught animals. Determining the RABV exposure history of a wild caught bat based on the presence or absence of viral neutralizing antibodies (VNA) may be misleading. Previous studies have demonstrated that the presence of VNA following natural or experimental inoculation is often ephemeral. With this knowledge, it is difficult to determine if a seronegative, wild caught bat has been previously exposed to RABV. The influence of prior rabies exposure in healthy, wild caught bats is unknown. To investigate the pathogenesis of RABV infection in bats born in captivity (naïve bats), naïve bats were inoculated intramuscularly with one of two Eptesicus fuscus rabies virus variants, EfV1 or EfV2. To determine the host response to a heterologous RABV, a separate group of naïve bats were inoculated with a Lasionycteris noctivagans RABV (LnV1). Six months following the first inoculation, all bats were challenged with EfV2. Our results indicate that naïve bats may have some level of innate resistance to intramuscular RABV inoculation. Additionally, naïve bats inoculated with the LnV demonstrated the lowest clinical infection rate of all groups. However, primary inoculation with EfV1 or LnV did not appear to be protective against a challenge with the more pathogenic EfV2.
doi:10.1371/journal.pone.0064808
PMCID: PMC3669413  PMID: 23741396
16.  Bat rabies surveillance in Finland 
Background
In 1985, a bat researcher in Finland died of rabies encephalitis caused by European bat lyssavirus type 2 (EBLV-2), but an epidemiological study in 1986 did not reveal EBLV-infected bats. In 2009, an EBLV-2-positive Daubenton’s bat was detected. The EBLV-2 isolate from the human case in 1985 and the isolate from the bat in 2009 were genetically closely related. In order to assess the prevalence of EBLVs in Finnish bat populations and to gain a better understanding of the public health risk that EBLV-infected bats pose, a targeted active surveillance project was initiated.
Results
Altogether, 1156 bats of seven species were examined for lyssaviruses in Finland during a 28–year period (1985–2012), 898 in active surveillance and 258 in passive surveillance, with only one positive finding of EBLV-2 in a Daubenton’s bat in 2009. In 2010–2011, saliva samples from 774 bats of seven species were analyzed for EBLV viral RNA, and sera from 423 bats were analyzed for the presence of bat lyssavirus antibodies. Antibodies were detected in Daubenton’s bats in samples collected from two locations in 2010 and from one location in 2011. All seropositive locations are in close proximity to the place where the EBLV-2 positive Daubenton’s bat was found in 2009. In active surveillance, no EBLV viral RNA was detected.
Conclusions
These data suggest that EBLV-2 may circulate in Finland, even though the seroprevalence is low. Our results indicate that passive surveillance of dead or sick bats is a relevant means examine the occurrence of lyssavirus infection, but the number of bats submitted for laboratory analysis should be higher in order to obtain reliable information on the lyssavirus situation in the country.
doi:10.1186/1746-6148-9-174
PMCID: PMC3846527  PMID: 24011337
EBLV; Lyssavirus; Rabies; Seroprevalence
17.  STUDIES ON THE PATHOGENESIS OF RABIES IN INSECTIVOROUS BATS  
Studies on the influence of environmental temperature on the pathogenesis of rabies in two species of experimentally infected Chiroptera, the Mexican free-tailed bat (Tadarida mexicana) and the little brown bat (Myotis lucifugus), provided evidence that little or no viral multiplication occurs in the inactive host during experimentally induced hibernation. When inoculated animals are wakened from hibernation by transfer to a warm room, virus previously in "cold storage" multiplies, reaching detectable levels in various tissues. Similar results were obtained with two strains of rabies virus, a canine rabies street virus which produced a fatal infection in man and a strain isolated from the pooled brown fat of naturally infected little brown bats. However, certain differences in the characteristics of these virus strains were observed. The canine rabies virus strain produced an encephalitic disease in mice and overt symptoms in bats; the bat rabies virus producing an encephalomyelitic disease in mice and infrequent symptoms in bats. The bat rabies virus had a greater predilection for brown adipose tissue than the canine strain. Results obtained with the bat rabies virus in hibernating animals indicate that after a period of latency in a dormant animal activated virus may reach the salivary gland more rapidly, with greater frequency, and attain higher concentrations than in animals which have not experienced a period of hibernation. The significance of these results as they relate to the natural history of bat rabies is discussed.
PMCID: PMC2137247  PMID: 19867178
18.  First Human Rabies Case in French Guiana, 2008: Epidemiological Investigation and Control 
Background
Until 2008, human rabies had never been reported in French Guiana. On 28 May 2008, the French National Reference Center for Rabies (Institut Pasteur, Paris) confirmed the rabies diagnosis, based on hemi-nested polymerase chain reaction on skin biopsy and saliva specimens from a Guianan, who had never travelled overseas and died in Cayenne after presenting clinically typical meningoencephalitis.
Methodology/Principal Findings
Molecular typing of the virus identified a Lyssavirus (Rabies virus species), closely related to those circulating in hematophagous bats (mainly Desmodus rotundus) in Latin America. A multidisciplinary Crisis Unit was activated. Its objectives were to implement an epidemiological investigation and a veterinary survey, to provide control measures and establish a communications program. The origin of the contamination was not formally established, but was probably linked to a bat bite based on the virus type isolated. After confirming exposure of 90 persons, they were vaccinated against rabies: 42 from the case's entourage and 48 healthcare workers. To handle that emergence and the local population's increased demand to be vaccinated, a specific communications program was established using several media: television, newspaper, radio.
Conclusion/Significance
This episode, occurring in the context of a Department far from continental France, strongly affected the local population, healthcare workers and authorities, and the management team faced intense pressure. This observation confirms that the risk of contracting rabies in French Guiana is real, with consequences for population educational program, control measures, medical diagnosis and post-exposure prophylaxis.
Author Summary
Until 2008, rabies had never been described within the French Guianan human population. Emergence of the first case in May 2008 in this French Overseas Department represented a public health event that markedly affected the local population, healthcare workers and public health authorities. The antirabies clinic of French Guiana, located at Institut Pasteur de la Guyane, had to reorganize its functioning to handle the dramatically increased demand for vaccination. A rigorous epidemiological investigation and a veterinary study were conducted to identify the contamination source, probably linked to a bat bite, and the exposed population. Communication was a key factor to controlling this episode and changing the local perception of this formerly neglected disease. Because similar clinical cases had previously been described, without having been diagnosed, medical practices must be adapted and the rabies virus should be sought more systematically in similarly presenting cases. Sharing this experience could be useful for other countries that might someday have to manage such an emergence.
doi:10.1371/journal.pntd.0001537
PMCID: PMC3283561  PMID: 22363830
19.  Immune sera and antiglycoprotein monoclonal antibodies inhibit in vitro cell-to-cell spread of pathogenic rabies viruses. 
Journal of Virology  1987;61(10):3314-3318.
Although the cell-to-cell spread of many viruses in vitro is inhibited by antibody, the effect of antibody on such spread of rabies viruses is uncertain. Thus, we examined the effects of anti-rabies virus immune sera and monoclonal antibodies (MAbs) on the in vitro spread of pathogenic rabies viruses in neuronal and nonneuronal cells. Both anti-rabies virus immune sera and neutralizing antiglycoprotein MAbs inhibited the cell-to-cell spread of street rabies virus, challenge virus standard, and ERA rabies viruses in cultures of neuroblastoma cells and of nonneuronal BHK-21 and chicken embryo-related cells. Furthermore, the cell-to-cell spread of virus was inhibited by greater than or equal to 75% with less than 1 IU/ml of human antirabies immunoglobulin. Nonneutralizing antinucleocapsid MAbs did not inhibit viral spread. After the immune serum was removed from the monolayers, virus spread rapidly to uninfected cells. Thus, antibody controlled the cell-to-cell spread of the virus but did not eliminate it from the cultures. Because antibody was more effective in inhibiting viral spread in fibroblast and epithelioid cells than in neuroblastoma cells infected at a high multiplicity of infection, we suggest that the inhibition of viral cell-to-cell spread by antibody in vivo would more likely occur at an initial site of exposure and before nerves are infected.
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PMCID: PMC255916  PMID: 3625841
20.  European Bat Lyssaviruses, the Netherlands 
Emerging Infectious Diseases  2005;11(12):1854-1859.
Genotype 5 lyssaviruses are endemic in the Netherlands, and can cause fatal infections in humans.
To study European bat lyssavirus (EBLV) in bat reservoirs in the Netherlands, native bats have been tested for rabies since 1984. For all collected bats, data including species, age, sex, and date and location found were recorded. A total of 1,219 serotine bats, Eptesicus serotinus, were tested, and 251 (21%) were positive for lyssavirus antigen. Five (4%) of 129 specimens from the pond bat, Myotis dasycneme, were positive. Recently detected EBLV RNA segments encoding the nucleoprotein were sequenced and analyzed phylogenetically (45 specimens). All recent serotine bat specimens clustered with genotype 5 (EBLV1) sequences, and homologies within subgenotypes EBLV1a and EBLV1b were 99.0%–100% and 99.2%–100%, respectively. Our findings indicate that EBLVs of genotype 5 are endemic in the serotine bat in the Netherlands. Since EBLVs can cause fatal infections in humans, all serotine and pond bats involved in contact incidents should be tested to determine whether the victim was exposed to EBLVs.
doi:10.3201/eid1112.041200
PMCID: PMC3367619  PMID: 16485470
EBLV; lyssavirus; the Netherlands; bat; Eptesicus serotinus; Myotis dasycneme; Europe; research
21.  Bat Rabies in Canada 1963-1967 
Six hundred and twenty-eight insectivorous bats originating from seven provinces were submitted to this Institute for rabies diagnosis between August 1, 1963 and December 31, 1967. Brain tissue was examined by the fluorescent antibody technique and the mouse infectivity test was carried out with brain, salivary gland, interscapular adipose tissue and kidney samples. Rabies virus was detected in 44 bats, 29 of which were from Ontario, 12 from British Columbia and three from Manitoba. Most of the positive cases were diagnosed in summer months. Seven species were represented among the specimens found to be rabid; there were 32 big brown bats, three hoary bats, three silver-haired bats, two little brown bats, one eastern pipistrelle, one Keen myotis and one red bat. Another bat which was not identified also proved to be infected with rabies.
PMCID: PMC1319378  PMID: 4242773
22.  Molecular Diversity of Rabies Viruses Associated with Bats in Mexico and Other Countries of the Americas 
Journal of Clinical Microbiology  2006;44(5):1697-1710.
Bat rabies and its transmission to humans and other species in Mexico were investigated. Eighty-nine samples obtained from rabid livestock, cats, dogs, and humans in Mexico were studied by antigenic typing and partial sequence analysis. Samples were further compared with enzootic rabies associated with different species of bats in the Americas. Patterns of nucleotide variation allowed the definition of at least 20 monophyletic clusters associated with 9 or more different bat species. Several lineages associated with distinctive antigenic patterns were found in rabies viruses related to rabies in vampire bats in Mexico. Vampire bat rabies virus lineages associated with antigenic variant 3 are widely spread from Mexico to South America, suggesting these lineages as the most likely ancestors of vampire bat rabies and the ones that have been moved by vampire bat populations throughout the Americas. Rabies viruses related to Lasiurus cinereus, Histiotus montanus, and some other not yet identified species of the genus Lasiurus were found circulating in Mexico. Long-range dissemination patterns of rabies are not necessarily associated with migratory bat species, as in the case of rabies in Desmodus rotundus and Histiotus montanus. Human rabies was associated with vampire bat transmission in most cases, and in one case, rabies transmission from free-tailed bats was inferred. The occurrence of rabies spillover from bats to domestic animals was also demonstrated. Genetic typing of rabies viruses allowed us to distinguish trends of disease dissemination and to address, in a preliminary fashion, aspects of the complex evolution of rabies viruses in different host-reservoir species.
doi:10.1128/JCM.44.5.1697-1710.2006
PMCID: PMC1479161  PMID: 16672396
23.  Enhanced Passive Bat Rabies Surveillance in Indigenous Bat Species from Germany - A Retrospective Study 
In Germany, rabies in bats is a notifiable zoonotic disease, which is caused by European bat lyssaviruses type 1 and 2 (EBLV-1 and 2), and the recently discovered new lyssavirus species Bokeloh bat lyssavirus (BBLV). As the understanding of bat rabies in insectivorous bat species is limited, in addition to routine bat rabies diagnosis, an enhanced passive surveillance study, i.e. the retrospective investigation of dead bats that had not been tested for rabies, was initiated in 1998 to study the distribution, abundance and epidemiology of lyssavirus infections in bats from Germany. A total number of 5478 individuals representing 21 bat species within two families were included in this study. The Noctule bat (Nyctalus noctula) and the Common pipistrelle (Pipistrellus pipistrellus) represented the most specimens submitted. Of all investigated bats, 1.17% tested positive for lyssaviruses using the fluorescent antibody test (FAT). The vast majority of positive cases was identified as EBLV-1, predominately associated with the Serotine bat (Eptesicus serotinus). However, rabies cases in other species, i.e. Nathusius' pipistrelle bat (Pipistrellus nathusii), P. pipistrellus and Brown long-eared bat (Plecotus auritus) were also characterized as EBLV-1. In contrast, EBLV-2 was isolated from three Daubenton's bats (Myotis daubentonii). These three cases contribute significantly to the understanding of EBLV-2 infections in Germany as only one case had been reported prior to this study. This enhanced passive surveillance indicated that besides known reservoir species, further bat species are affected by lyssavirus infections. Given the increasing diversity of lyssaviruses and bats as reservoir host species worldwide, lyssavirus positive specimens, i.e. both bat and virus need to be confirmed by molecular techniques.
Author Summary
According to the World Health Organization rabies is considered both a neglected zoonotic and a tropical disease. The causative agents are lyssaviruses which have their primary reservoir in bats. Although bat rabies is notifiable in Germany, the number of submitted bats during routine surveillance is rarely representative of the natural bat population. Therefore, the aim of this study was to include dead bats from various sources for enhanced bat rabies surveillance. The results show that a considerable number of additional bat rabies cases can be detected, thus improving the knowledge on the frequency, geographical distribution and reservoir-association of bat lyssavirus infections in Germany. The overall proportion of positives was lower than during routine surveillance in Germany. While the majority of cases were found in the Serotine bat and characterized as European bat lyssavirus type 1 (EBLV-1), three of the four EBLV-2 infections detected in Germany were found in Myotis daubentonii during this study.
doi:10.1371/journal.pntd.0002835
PMCID: PMC4006713  PMID: 24784117
24.  Bat Rabies in British Columbia 1971-1985 
Rabies virus was demonstrated in 99 of 1154 bats submitted from British Columbia between 1971 and 1985. Rabies was diagnosed in seven species including big brown bats (Eptesicus fuscus), the latter accounting for 51% of all positive cases. Colonial species represented 92.9% of all identified bats and 87.7% of all rabid cases. Most bats were submitted from the more densely populated areas of the province, and submissions and positive cases both peaked in the month of August. Daytime activity and inability to fly were the most common behaviors reported in rabid bats.
PMCID: PMC1680738  PMID: 17422945
25.  Genetic characterization of rabies field isolates from Venezuela. 
Journal of Clinical Microbiology  1996;34(6):1553-1558.
Twenty samples from cases of rabies in humans and domestic animals diagnosed in Venezuela between 1990 and 1994 and one sample from a vampire bat collected in 1976 were characterized by reactivity to monoclonal antibodies against the viral nucleoprotein and by patterns of nucleotide substitution in the nucleoprotein gene. Three antigenic variants were found: 1, 3, and 5. Antigenic variant 1 included all samples from dogs and humans infected by contact with rabid dogs. Unique substitutions permitted identification of two separate outbreaks of dog rabies in the Maracaibo Depression and Los Llanos region and in the Andean region of Venezuela. Samples from the vampire bat and two head of cattle were characterized as antigenic variant 3 and showed a nucleotide sequence homology of 96 to 98% to each other and to samples of vampire bat-associated rabies throughout Latin America. Ten of the remaining 12 samples were characterized as antigenic variant 5. Genetic studies indicated that 11 of these samples formed a highly homologous and distinctive group but were closely related to samples of vampire bat-associated rabies. The 12th sample of variant 5 (from a cat) showed only 78 to 80% genetic homology to samples of rabies associated with vampire bats. The application of antigenic and genetic typing to rabies surveillance in Latin America is essential to improve control programs. Recognition of the source of outbreaks of dog rabies and identification of wildlife species maintaining sylvatic cycles of rabies transmission permit better utilization of public health resources.
PMCID: PMC229062  PMID: 8735118

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