key: cord-0757530-elxapr7a authors: Harris, S.L.; Brookes, S.M.; Jones, G.; Hutson, A.M.; Racey, P.A.; Aegerter, J.; Smith, G.C.; McElhinney, L.M.; Fooks, A.R. title: European bat lyssaviruses: Distribution, prevalence and implications for conservation date: 2006-06-06 journal: Biol Conserv DOI: 10.1016/j.biocon.2006.04.006 sha: 1fa2b0b3e60ed67e77878cff264b50016515c687 doc_id: 757530 cord_uid: elxapr7a Worldwide, there are more than 1100 species of the Order Chiroptera, 45 of which are present in Europe, and 16 in the UK. Bats are reservoirs of, or can be infected by, several viral diseases, including rabies virus strains (in the Lyssavirus genus). Within this genus are bat variants that have been recorded in Europe; European bat lyssavirus 1 (EBLV-1), European bat lyssavirus 2 (EBLV-2) and, four currently unclassified isolates. Since 1977, 783 cases of EBLVs (by isolation of viral RNA) have been recorded in Europe. EBLV-1 or EBLV-2 has been identified in 12 bat species, with over 95% of EBLV-1 infections identified in Eptesicus serotinus. EBLV-2 is associated with Myotis species (Myotis daubentonii and Myotis dasycneme). A programme of passive surveillance in the United Kingdom between 1987 and 2004 tested 4871 bats for lyssaviruses. Of these, four M. daubentonii (3.57% of submitted M. daubentonii) were positive for EBLV-2. Potential bias in the passive surveillance includes possible over-representation of synanthropic species and regional biases caused by varying bat submission numbers from different parts of the UK. In 2003, active surveillance in the UK began, and has detected an antibody prevalence level of 1–5% of EBLV-2 in M. daubentonii (n = 350), and one bat with antibodies to EBLV-1 in E. serotinus (n = 52). No cases of live lyssavirus infection or lyssavirus viral RNA have been detected through active surveillance. Further research and monitoring regarding prevalence, transmission, pathogenesis and immunity is required to ensure that integrated bat conservation continues throughout Europe, whilst enabling informed policy decision regarding both human and wildlife health issues. In this paper we present an overview of lyssavirus strains that are found in bat species, focussing on European bat lyssaviruses. We will then compare surveillance strategies for lyssaviruses, and in particular those within the UK are discussed. Finally, we will highlight the implications for both bat conservation and human health risks. In this section of the review, we introduce the order Chiroptera, and the legislation currently protecting bats species in Europe. Viral diseases currently recorded in bats, the importance of differential diagnosis and lyssavirus detection methods are also discussed. Recent research on the molecular phylogeny of bats places the origins of the Order Chiroptera in the early Palaeocene (64 million years ago) during a period of significant global warming (Simmons, 2005a; Teeling et al., 2005) . Of all known extant mammal species, 20% are bats, the only mammals capable of powered flight. Bats are found on every continent except Antarctica, and more than 1100 surviving bat species exist world-wide (Simmons, 2005b) . Of the 19 families found worldwide, five are represented in Europe (Vespertilionidae, Rhinolophidae, Molossidae, Emballonuridae, Pteropodidae) (Table 1) , with 45 bat species currently listed as European residents including 16 (Myotis myotis is believed to be extinct in the UK as a breeding population) in the UK (EUROBATS, 2004a; Dietz and von Helversen, 2004 ). Data from EUROBATS (2004a) , and Dietz and von Helversen (2004) . a The number of European bat species is taken from the EUROBATS (2004a) Protected Species list. The list of countries used to define Europe in this instance, is also taken EUROBATS (EUROBATS, 2004b) . b UK status taken from Harris et al. (1995) . c Myotis myotis is believed to be extinct as a breeding population in the UK. In 1975, the Wild Creatures and Wild Plants Act protected the two most endangered bat species, Rhinolophus ferrumequinum and M. myotis (Racey, 1992) . All bats and their roosts are protected in the UK under the provisions of the Wildlife and Countryside Act (WCA) 1981, which provides the legal framework for bat-related legislation and implementation in the UK for both the Bern Convention (1982) and the Bonn Convention (1985) . In England and Wales the provisions of the WCA have recently been strengthened through the Countryside and Rights of Way (CROW) Act, 2000. In addition, the UK ratified EUROBATS in September 1992. Certain bat species are also listed on Annex II (and all species on Annex IV) of the European Habitats Directive. As of July 2004, the UK had recommended 42 maternity and hibernacula areas as Special Areas of Conservation (SACs), and 93 areas as candidate Special Areas of Conservation (cSACs) under the Habitats Directive. Bat species were either the main reason for an area's recommendation, or a qualifying feature. Implementation of the UK Biodiversity Action Plan (BAP) also includes action for six bat species and the habitats that support them, in the form of Species Action Plans (SAPs) (JNCC, 1998 (JNCC, -2005 . Ten virus families, including lyssaviruses, have been isolated in bats (Table 2 ) (Messenger et al., 2003b) . There are currently seven virus genotypes (Table 3) in the Lyssavirus genus (family Rhabdoviridae). The genotypes that have been recorded in bats include classical rabies virus (RABV), Lagos bat virus (LBV), Duvenhage virus (DUVV), the European bat viruses (EBLV-1 and EBLV-2) and the Australian bat virus (ABLV). In addition, four viruses that have been isolated from bats are currently awaiting classification in the Lyssavirus genus. These are Aravan virus (ARAV) Botvinkin et al., 2003; Kuzmin et al., 2003) , Khujand virus (KHUV), West Caucasian Bat virus (WCBV), and Irkut virus (IRKV) Kuzmin et al., 2005) . Only one Lyssavirus genotype, Mokola virus (MOKV), has never been isolated from bats. Rabies can be caused by any of the genotypes within the Lyssavirus genus. It is a fatal disease of the central nervous WHO, 2006) , with infection resulting in a wide variety of neurological symptoms. In bats, clinical signs of rabies include weight loss, lack of coordination, muscular spasms, agitation, increased vocalisation and overt aggression (Barrett et al., 2005; Bruijn, 2003; Johnson et al., 2003; Shanker et al., 2004; Whitby et al., 2000) . Rabies may be suspected when bats exhibit unusual behavioural signs or unexplained paralysis, but clinical indications of rabies in bats can be variable and are not always characteristic. Bats may also be chronic asymptomatic carriers ( (Lane, 1999) . Lead poisoning has been documented in fruit bats in Australia (Sutton and Wilson, 1983) . Signs presented included severe muscle fasciculation, inability to fly, excessive salivation, ataxia, and making distress noises when approached or handled. Indeed, lead poisoning has been reported in conjunction with ABLV in frugivorous bats and the ABLV initially went undiagnosed because the poisoning was thought to cause the signs presented (Skerratt et al., 1998) . However, lead poisoning was also mistaken for rabies in a dog in Australia (Animal Health Australia, 2000) . Poisoning by blue-green algae has been reported in bats (WHO, 1998) , usually resulting in hepatotoxity. The toxins involved include anatoxin-a, a hepatotoxin which leads to convulsions, staggering, abnormal posturing and arching of the back (Codd et al., 2003) . As with viruses, many bacteria can give rise to encephalitis, and therefore altered neurological signs. Little is known about the normal bacterial flora of bats, but pathogenic bacteria have occasionally been isolated. Listerial encephalitis has been mistaken for rabies in cattle in Australia (Animal Health Australia, 2000) , whilst Listeria induced 'circling disease' is common in sheep, and has been seen concurrently with EBLV in Denmark (Ronsholt, 2002; Tjørnehøj et al., 2006) . Fatal meningoencephalitis associated with Listeria monocytogenes has also been seen in fruit bats (Hohne et al., 1975) . Brucella species can also cause meningoencephalitis and CNS disease in humans and animals (Sohn et al., 2003) , and anti-Brucella agglutins have been found in vampire bats (Ricciardi et al., 1976) . Neurological disease has been documented in Australian species of Old World fruit bats caused by the helminth Angiostrongylus cantonensis. Signs included anorexia, hind limb weakness/paralysis, and tetraplegia. Post-mortem examination revealed severe meningoencephalitis (Reddacliff et al., 1999) . Post-mortem diagnosis (including laboratory tests) must therefore be undertaken to exclude notifiable and exotic diseases such as rabies. In the UK, rabies is a notifiable disease in man ( 1.6. In general, rabies is diagnosed in many laboratories following positive microscopic examination of brain tissue by the direct fluorescent antibody test (FAT), which employs the immunodetection of the virus nucleocapsid protein (Dean et al., 1996; Kamolvarin et al., 1993) . The reverse transcriptase (RT) polymerase chain reaction (PCR) can be used to detect the presence of pan-lyssa virus RNA. Nested primers for pan-lyssa virus or primers specific for EBLVs can be effectively used for the detection of low levels of viral RNA, especially from non-invasive samples including saliva (Heaton et al., 1997; Johnson et al., 2002) . Virus isolation is performed using a homogenised suspension of suspect tissue (normally brain tissue) or from saliva (Noah et al., 1998) by either the rabies tissue culture inoculation test (RTCIT) or the mouse inoculation test (MIT) (Koprowski, 1996; Webster and Casey, 1996) . Table 4 summarises the distribution of virus throughout lyssavirus positive bats. The brains of all of the bats were positive as determined by one or more of the techniques given above, with other tissues positive in one or more reports, although not all tissues were examined in all cases. In addition, detection of virus in the brown fat of bats has been implicated in possible chronic infection of bats during hibernation (Sulkin et al., 1959; Nilsson and Negata, 1975 ). In this section, we provide a review of European bat lyssavirus cases (both human and animal), their geographic distribution and implemented surveillance strategies across Europe, including the UK in detail. Other Lyssavirus genotypes are also described. The presence of EBLVs in Europe was first documented in 1954 (Kappelar, 1989; King et al., 2004) , and during the period 1977-2004, 783 EBLV confirmed cases (by isolation of viral RNA) have been reported (King et al., 2004; Mü ller, 2000; Rabies Bulletin Europe, 2001 , 2003 . EBLV-1 (genotype 5) and EBLV-2 (genotype 6) are related to, but can be genetically and antigenically distinguished from classical rabies (RABV: genotype 1) (Bourhy et al., 1992 (Bourhy et al., , 1993 (Bourhy et al., , 1999 Badrane et al., 2001) . In addition, both EBLVs can be distinguished from each other using sequence analysis of the N and/or G genes (Fooks et al., 2003a ). EBLV-1 is present in Europe in two lineages, EBLV-1a and EBLV-1b. EBLV-1a is thought to be the most recently introduced from North Africa via southern Spain, and exhibits an eastwest European division. The distribution of EBLV-1b appears to follow a north-south division. The Netherlands and France are the only countries in which both EBLV-1a and EBLV-1b have been found (Amengual et al., 1997; Picard-Meyer et al., 2004a,b; Van der Poel et al., 2005) . The majority (>95%) of the 750 EBLV-1 cases in European bats have been identified in one bat species, Eptesicus serotinus (Table 5) , which should therefore be regarded as the most likely reservoir species. E. serotinus is found both in the UK and mainland Europe (Stebbings and Robinson, 1992) . In the UK, it is found mainly south of a line from The Wash (East Anglia) to south Wales (Hutson, 1991) . It is widespread across western Europe, north to Denmark and southern Sweden, south to North Africa, eastwards to the Himalayas and north to Korea, possibly expanding its range in Europe (Baagøe and Jensen, 1973; Baagøe, 2001 ). This species is not commonly migratory, but movements of up to 330 km (200 miles), have been recorded from eastern Europe (Stebbings and Griffith, 1986; Baagøe, 2001; Strelkov, 1969) . Active infection (replicating virus in the CNS and/or excretion of virus in saliva) caused by EBLV-1 has not been recorded in the UK to date, and the disparity between EBLV-1 records in Europe and the UK may be related to the limited geographical distribution and population size of E. serotinus within the UK. Spillover of EBLV-1 (Table 6 ) into sheep has occurred on two separate occasions in Denmark, in 1998 (Ronsholt, 2002 Tjørnehøj et al., 2006) , and into a stone marten in Germany (Mü ller et al., 2001) , a domestic cat (antibodies only) in Denmark (Tjørnehøj et al., 2004) and one confirmed human case (Selimov et al., 1989; Bourhy et al., 1992) . A further two unconfirmed human cases of suspected bat origin have also been reported ( EBLV-2 was first isolated in 1985 from a human, (a Swiss bat biologist) who had been working with bats in Finland, Switzerland and Malaysia (Lumio et al., 1986) . In 1986, EBLV-2 was isolated in Denmark and Germany from Myotis daubentonii and in Denmark from M. dasycneme (Table 5) , the only known natural (1986) 1986-1987 Eptesicus serotinus 150 EBLV-1 Grauballe et al. (1987 Grauballe et al. ( ) 1986 Myotis dasycneme, Myotis daubentonii 2 EBLV-2 King et al., 1994 King et al., 1987 Myotis daubentonii 1 EBLV-2 King et al., 1994 King et al., 1998 King et al., -2001 Not (Stebbings and Griffith, 1986; Roer, 2001; Limpens et al., 2000; Roer and Schober, 2001) . In the UK, four cases of EBLV-2 have been identified in M. daubentonii ( Table 5) . Two of the four bats were reported as having bitten humans, and one was reported as being brought into a domestic residence by a cat. Of the four UK cases, two originated in the county of Lancashire (2002, 2004) , one in Sussex (1996) , and one in Surrey (2004). Both counties of Lancashire and Sussex have submitted a substantially higher proportion of M. daubentonii than other counties for passive surveillance testing. This perhaps indicates that high numbers of bats (of a given species) submitted for rabies testing from specific geographical regions increases the probability of identifying positive cases. Positive results, establishing the presence of EBLV-2 in all four bats' brains, were obtained by FAT, RTCIT and MIT. Identification of the genotype in each case was undertaken by PCR and sequencing of the nucleoprotein gene and shown to be EBLV-2. Spillover of EBLV-2 to humans (Table 6 ) has occurred twice, in Finland in 1985 (Lumio et al., 1986) and in the UK in 2002 (Fooks et al., 2003b) . EBLV-2 Spillover into other animal species has not yet been documented. In specific European countries, EBLV infection is currently monitored by passive surveillance of dead or ill bats, using a variety of detection methods (King et al., 2004) . In some countries, risk or indicator species are regularly tested where clinical signs are well known and recorded. Table 5 gives the recorded cases of EBLV in bats across Europe by country (where positive cases are documented by laboratory analysis testing for viral RNA in brain or saliva samples). Financial resources also play a significant role in the scope and surveillance abilities of different countries, with testing density and sample volume being directly affected by financial resources, through the co-financing scheme of the EU (Potzsch, 2004) . If the rabies-free status of any European country is to be maintained, then susceptible terrestrial animals must be shown to be both disease-and exposure-free. Effective surveillance is a vital component of any policy that helps to maintain the rabies-free (virus/disease) status of a specific country. The apparent lack of EBLV surveillance in some areas of Europe may be due to classical rabies in fox populations being seen as having greater direct importance, both economically and for public health (Warrell and Warrell, 2004) . The WHO defines an area as 'rabies-free' where an effective import policy is implemented, and where the area is currently free of indigenous rabies in terrestrial mammals, with no new indigenous case being reported for a period of two years. Currently the Office International des Epizooties (OIE) ex-cludes bat rabies when declaring a country rabies-free (Mü ller, 2002) . During the period 1985-1987, there was a noticeable increase in the number of bats submitted for rabies testing within Europe. The increase in submission numbers of bats, the human case of EBLV-2 in Finland in 1985, and a biting incident involving E. serotinus in Denmark in 1985 (MMWR, 1986) led to EBLV surveillance being taken more seriously. Concern that the disease could be introduced into the UK by bats crossing from mainland Europe led to a programme of screening dead bats for the presence of lyssaviruses. This was initiated at the Rabies Research and Diagnostic Unit at the Veterinary Laboratory Agency (VLA: formerly Central Veterinary Laboratory). The passive surveillance programme has been in place since 1987. Dead bats are sent to the VLA by members of the public, or more frequently, by members of the UK's local bat groups. The annual total of submissions, and the number of submissions for each species between 1987 and 2004, including sex and age ratios are given in Table 7 . The average number of bats sent to the VLA each year since 1987 is 270 (range 96-898). However, passive surveillance is likely to have several inherent biases. First, the habitat and colony preference of individual species is thought to have an effect on how frequently they are found by the general public. For example, Pipistrellus species (P. pipistrellus/Pipistrellus pygmaeus) and E. serotinus utilize houses for maternity colonies, increasing the likelihood of grounded adults or young being found. M. daubentonii frequently uses tree cavities during the summer, and caves and mines in the winter, and is therefore far less likely to come into contact with members of the public. This means that some species, when compared to the most recent UK species population estimates, are being under-or over-represented by passive surveillance (Table 8) . Second, successful passive surveillance is dependent on bats being recovered from a geographical range that mirrors their natural distribution. In the UK, there are over 90 volunteer bat groups creating a UK wide network, but the activity of these groups and their geographic locations are not necessarily uniform across the UK. Eighty three percent of bats (1987) (1988) (1989) (1990) (1991) (1992) (1993) (1994) (1995) (1996) (1997) (1998) (1999) (2000) (2001) (2002) (2003) (2004) have been sent in from England (n = 4041), 8.7% from Scotland (n = 426), 3.5% from Wales (n = 172), with the remaining bats sent from Northern Ireland (n = 15), Republic of Ireland (n = 1), Channel Islands (n = 32), UK offshore (n = 1), and those of unknown origin (n = 185). This has created regions of the UK where very few bats, of few species, have been tested (VLA, unpublished data). Since the detection of EBLV-2 in a M. daubentonii bat in Sussex (1996) , the Bat Conservation Trust (BCT) has been working in collaboration with the Department for Environment, Food and Rural Affairs (Defra) and the VLA to promote both the importance of testing bats for EBLVs, and the essential role of the local bat groups. The annual total for bat submission under the passive surveillance scheme have reflected the pattern of UK EBLV cases, with a substantial increase in submissions in the period following each positive case (Harris et al., 2006) . Following the EBLV-2 positive UK bat case in 1996, concern over the potential bias in passive surveillance, and an increased reporting of EBLV in certain bat species in Europe, it Sampling has focussed on M. daubentonii and E. serotinus, as these are the two main bat species resident in the UK that are known reservoirs of EBLVs in continental Europe, although other species have been sampled in small numbers. The active surveillance sampling tests for both previous exposure (antibody levels), and current infection (viral excretion in saliva). Data generated from two locations (within the counties of Angus and Lancashire) where there was an a priori reason to believe that antibody positive bats would be found, gave a prevalence estimate (for M. daubentonii) of approximately 8%, with a 95% CI of between 3 and 16%. In contrast, the data from all the other sites in England and Scotland (n = 25) suggests that approximately 2% of the M. daubentonii population is antibody positive, with a 95% CI of between 1% and 5% Brookes et al., 2005a) . From the 52 E. serotinus tested by a virus neutralization assay (mFAVN), one sample gave an EBLV-1 positive antibody result (VLA, unpublished data). A longitudinal study (2005 onwards) will enable further sampling and analysis of antibody prevalence within the UK Serotine population. No oral swabs from bats (including those that were antibody positive) of any species tested during active surveillance were found to be RT-PCR positive for viral RNA, and no live virus was detected using RTCIT Brookes et al., 2005a) . The detection of virus neutralising antibody in blood samples reflects past exposure to EBLVs only, and does not demonstrate active infection (excretion of virus in saliva) at the time of sampling. The serum data collected 2003-2004, combined with the oropharyngeal swab results may imply that the bats had elicited a sufficient immune response to suppress the virus and might therefore remain sero-positive without excreting virus in saliva. It is probable that bats excreting virus are more likely to show atypical behavioural changes when caught in the field (Johnson et al., 2003) . Therefore, not finding EBLV-2 viral RNA in saliva samples from bats that were antibody positive was not unexpected (Brass, 1994) . Additionally, the excretion of RABV at least is known to vary with time, an infected animal can excrete virus one day and not the nextso the bat would have to be excreting virus at the time of swabbing for us to be able to detect it. All of the bats that were sampled appeared to be healthy, and were not exhibiting obvious clinical signs of rabies. The majority of the M. daubentonii sampled were caught on the wing, another indication of relative good health, considering that active infection in bats may lead to paralysis. The E. serotinus sampled were caught both on the wing, and in some cases, taken by hand from their day-roost locations. Therefore, ability to fly was not always observed before sampling of E. serotinus occurred. Further sampling is required on both principal target species (E. serotinus and M. daubentonii), at both 'a priori' sites and other sites where there is no reason to expect antibody positive bats. It is clear that some bat populations (at least M. daubentonii) are routinely exposed to lyssaviruses in the UK, and that EBLV-2 has probably been established in the UK for some considerable time. Potentially risks therefore exist for humans and other animals, and an important challenge is to minimize these risks while promoting the conservation of bats. Before addressing how these issues can be reconciled, we will review the distribution of other lyssaviruses in bats, and mechanisms of virus transmission from bats. Other lyssaviruses in bats 3.1. Classical rabies (RABV -genotype 1) Classical rabies was first recorded in insectivorous bats in Brazil in the 1920s (Baer and Smith, 1991) and in frugivorous bats in 1931, in Trinidad (Pawan, 1936a,b) , but has never been recorded in native European bat species; EBLVs are thought to fill this ecological niche (Table 3) . In North America, the highest prevalence of RABV in wild animals is reported in carnivores (foxes, racoons, skunks), but RABV has been recorded from species in other orders of mammal. The first recording of RABV in North America in an insectivorous bat was in 1951 (King et al., 2004) , and since then it has been documented from all over North America (Cliquet and Picard-Meyer, 2004) . The annual average prevalence of RABV (viral RNA detection) in bats tested (dead or moribund bats) from nine states of North America between 1988 and 1992 was 7.4% (n = 192/2583). The bat species most commonly submitted are Eptesicus fuscus, Myotis lucifugus, Lasiurus borealis, Lasiurus blossevilli, and Tadarida brasiliensis. The prevalence of RABV infection in submitted bats was lowest in M. lucifugus (1.2%), and highest in L. cinereus and T. brasiliensis, both at 24% (Smith et al., 1995) . Surveillance studies indicate a prevalence of rabies virus in <1% of randomly sampled bats (viral RNA detection), and between 3% and 25% among bats submitted to state health departments (Brass, 1994; Schneider et al., 1957; Constantine, 1967a; Trimarchi and Debbie, 1977; Childs et al., 1994; Yancey et al., 1997; Trimarchi, 1998) . Of the total human RABV cases (35 cases during 1958-2000) , 19 have been linked with three insectivorous bat species, L. noctivagans (14 cases), Myotis species (two cases) and T. brasiliensis (three cases) in North America. In 1993, three cases of rabies of probable bat origin in red foxes Vulpes vulpes were confirmed on Prince Edward Island (Canada) (Daoust et al., 1996) . In 2001, 19 skunks from Arizona sent for rabies testing to the Texas Department of Health were found to be infected with a RABV variant more commonly identified in E. fuscus and Myotis species (Smith, 2001) . In Latin America, Desmodus rotundus, the common vampire bat, is thought to be the principal reservoir of RABV infections in humans (500 cases during 1975-2000) (McColl et al., 2000) . Cases of human RABV infection resulting from vampire bat species may be under-reported in Latin America, but several outbreaks have been recorded Milagres, 2005; Rodriguez, 2005) . Attacks by vampire bats appear to occur most frequently in areas of human settlement (Caraballo, 1996; Schneider, 1991; Schneider et al., 1996; Schneider and Uieda, 1998) , or when normal food sources are not available, such as following the removal of pigs during a hog cholera eradication campaign (McCarthy, 1989) . RABV of vampire bat origin in cattle is of economic concern, but has also led to significant losses of both habitat and bat species through ill-conceived bat control programmes. Lagos bat virus (LBV -genotype 2) was first isolated from the brain of the straw-coloured bat (Eidolon helvum) in 1956 (Lagos Island, Nigeria) (Boulger and Porterfield, 1958) , and has since been isolated from the same species in Senegal, in 1980 (Table 3 ). It has also been reported in other bat species for which limited information is available including Epomophorus wahlbergi and an unidentified bat species (both from the Natal Province, South Africa), Micropteropus pusillus (Central African Republic), and Nycteris gambiensis (Guinea). The case identified in E. wahlbergi in South Africa involved a rabies-like outbreak involving many bats of that species. Lagos bat virus has also been isolated from cats (Zimbabwe and Natal) and a dog (Ethiopia). There is no record of human infection (Brass, 1994) . In addition to these records, isolation of the virus was reported from a bat imported into France from either Togo or Ethiopia in 1999 (the origin of the bat was unconfirmed). The bat was recorded as a Pteropus species, but this genus does not occur on mainland Africa, and therefore was believed to have been mis-identified (Aubert, 1999; Hutson, 2004 ). Mokola virus was first isolated in 1968 in Nigeria from a shrew, and has since been recorded again from a species of white-toothed shrew (Crocidura species) (Cameroon), and once in the brush-furred mouse (Lophuromys sikapusi) (Central African Republic) ( Table 3) . Apart from these cases, the virus has been isolated from several domestic cats and a single dog in Zimbabwe. There have been two reported human cases both from Nigeria, one fatal, and the other case was believed to have been misdiagnosed (Brass, 1994) . Mokola virus is believed to be widespread, but uncommon is West Africa, Central Africa, Ethiopia, Zimbabwe and South Africa (Bingham et al., 2001) . The virus has not been recorded in any bat species, however they have been considered as a potential reservoir host (Shope et al., 1970; Brass, 1994) . Duvenhage virus was first isolated in 1970 (Table 3 ), in Transvaal, South Africa, from a fatal human case (Meredith et al., 1971) . This was believed at the time to have been caused by a bite from an insectivorous bat (either Miniopterus schreibersii or Miniopterus schreibersii natalensis), although the evidence for the bat bite has since been seen as circumstantial ( Van der Merwe, 1982) . The virus has subsequently been isolated from an unidentified insectivorous bat species (Transvaal, Africa in 1981) and from a Nycteris thebaica (Zimbawe in 1996) (Brass, 1994) . In 1996, ABLV was first isolated from a Pteropus alecto bat in New South Wales, Australia (Table 3) , and two human deaths were also reported in Australia that year (Allworth et al., 1996; Hanna et al., 2000) . During this time, ABLV was also isolated from two further fruit bat species (P. scapulatus and P. poliocephalus), and from an insectivorous species (Saccolaimus flaviventris). In 2000, contact between a wild P. alecto and a captive P. poliocephalus separated by wire-mesh resulted in transmission of ABLV. Subsequent modification of the enclosure prevented future direct contact between free-living wild bats and the captive colony (Warrilow et al., 2003) . Evidence of infection has been recorded in bats in all states except South Australia (Fraser et al., 1996; Tidemann et al., 1997; Hooper et al., 1997; Gould et al., 1998; Samaratunga et al., 1998) . A survey involving 119 bats linked with potential human contact cases, including various Pteropus species (n = 85) and nine insectivorous species (n = 34), found eight positives (by FAT) in Pteropus species, (prevalence estimate of 9.4% in submitted bats) and no positives in the other species. Opportunity for cross-species transmission of ABLV involving pteropodids may be partly facillitated by the large, seasonal, nomadic and sometimes multi-species colonies in which they are known to congregate (Warrilow et al., 2003) . In the Philippines, active surveillance of bats during the 1950s and 1960s failed to record active rabies infection, although surveillance in 1998 found a 9.5% ABLV antibody prevalence (n = 231), but no active infection (Arguin et al., 2002) . Active surveillance in Thailand found an antibody prevalence to ABLV between 4% and 7.3% (n = 394), (Lumlertdacha et al., 2005) . In this section we provide evidence for EBLV tolerance in bats, and discuss forms of transmission of EBLV from bats to humans. The apparent differences in virulence between Lyssavirus genotypes for different animal species will also be considered. There is an increasing body of evidence to suggest that bats tolerate lyssavirus infection. A study following the unexplained infection of a captive colony of Rousettus aegyptiacus with EBLV-1 (Ronsholt et al., 1998) , demonstrated that though the virus was pathogenic for the bat, this species could survive challenge with this virus (rabies antigen and neurological signs were detected in six out of seven of the 16 inoculated bats) ( Van der Poel et al., 2000) . Further studies revealed that up to 85% of apparently healthy colony members (n = 43) were seropositive for EBLV-1, indicating exposure to the virus (Wellenberg et al., 2002) . In a recent study, the EBLV-1 RNA was detected in a range of tissues from apparently healthy specimens of M. myotis, Myotis nattereri, R. ferrumequinum, and Myotis schreibersii. In the same study, neutralising antibodies were present in M. myotis, M. schreibersii, Tadarida teniotis and R. ferrumequinum (Serra-Cobo et al., 2002) . These studies corroborate investigations of bats endemic to Europe, which demonstrated, by repeated humane blood sampling of selected bat colonies, that the same seropositive individuals could be detected over a six-year period. This illustrates that bats may survive EBLV infection with possible long-term maintenance of virus in infected healthy individuals (Perez-Jorda et al., 1995; Echevarria et al., 2001; Serra-Cobo et al., 2002; O'Shea et al., 2003 O'Shea et al., , 2004 . However, it is not clear how EBLVs are transmitted between bats within a colony. The complex social behaviour of bats, sometimes including allogrooming (Kerth and Konig, 1999 ) may possibly enable virus dissemination through the sharing of saliva. It is speculated, however, that the mechanisms of EBLV transmission via the oral route and the level of viral load involved may result in a 'silent' (no obvious clinical signs) infection. The possibility exists that bats might act as 'asymptomatic viral carriers' resulting in a sub-clinical infection. Virus re-activation may also occur as a result of specific 'stress' factors including pregnancy, hibernation, nutritional deficit, and migration, that cause immunosup-pression and potentially increase rabies-related mortality (Sulkin et al., 1959 (Sulkin et al., , 1960 Sims et al., 1963; Constantine, 1967a,b) . Previous work (Soave, 1962 (Soave, , 1964 has shown that even after long periods of asymptomatic infections, guinea pigs developed clinical rabies when subjected to stress (Messenger et al., 2003a) . In contrast, as part of complex bat behaviour, biting incidents that may result in viral transmission are fairly common. Transmission could be followed by abortive peripheral infection via lack of virus replication or the development of sterilising immunity. Alternatively, the virus replicates locally, is transmitted to the CNS and fatal infection ensues. In 2001, a captive colony of 35 E. fuscus was created from wild-caught bats and held for just under five months to study the epidemiology and transmission of the classical rabies virus (RABV). Within the first month of capture, two bats died, and were found to be positive for RABV by RT-PCR of brain tissue, salivary gland and oral swabs. Of the remaining bats, all remained outwardly healthy, with two bats seroconverting whilst in captivity. Five other individuals that had been seropositive for RABV before capture, maintained their positive antibody levels (Shanker et al., 2004) . Cryptic transmission (cases where a clear history of exposure to rabies cannot be documented) of RABV bat variants to humans in the Americas is thought to occur once or twice each year; often the bite goes unrecognised (Jackson and Brock Fenton, 2001; Messenger et al., 2002 Messenger et al., , 2003b . It is feasible that in Europe viral encephalitis currently of unknown aetiology might occur following exposure as a result of a bite from an EBLV-infected bat Davison et al., 2003) . In the majority of cases of human rabies infection the source is a bite wound. In some cases however, infection may result from the virus coming into contact with mucous membranes (e.g. eyes, nose and mouth). There are four reported instances of human rabies following inhalation of aerosol virus, two cases in a laboratory (Winkler et al., 1973) , and two in a bat cave (Gibbons, 2002) . However, it cannot be shown conclusively, particularly with the cave infections, that there were no other means of infection, as one of the cavers involved was reported as having an open wound on his face (Constantine, 1962 (Constantine, , 1988a Brass, 1994; Gibbons, 2002) . However, airborne transmission of Lyssaviruses has been demonstrated experimentally (Johnson et al., 2006a) . There are also a small number of cases of fatal human rabies infection in recipients of donated organs (Hough et al., 1979; Srinivasan et al., 2005; Hellenbrand et al., 2005) . The potential for direct transmission of lyssavirus is indicated by the presence of virus in the salivary glands, tongue and pharynx. These organs appear to be the most significant in relation to the most common forms of virus spread; bite, lick (on broken skin) or contact with mucous membranes. All three confirmed human cases of EBLV documented previous exposure to bat bites. The human case of rabies caused by EBLV-1 reported a specific biting incident from a single bat. The two human cases of rabies caused by EBLV-2 reported multiple exposures to bats involving biting incidents. It is possible that EBLV transmission may occur infrequently due to low levels of virus in saliva, poor invasive ability of EBLVs, or immune status of those bitten (Fooks et al., 2003a) . This suggests that bat to human spread of EBLVs may require a significantly higher viral load before an active infection is established compared to the virus load received from a dog bite. However, the extent and depth of exposure (physical area of exposure and amount of saliva) in dog bites is generally much greater than that of bat bites. In a comparison of two RABV isolates (a L. noctivagans isolate taken from a naturally infected human from California, and a coyote street virus isolate taken from a naturally infected coyote from Texas) from North America, the isolate from L. noctivagans replicated to higher titre levels in epithelial and fibroblast cells at cooler temperatures (34°C) (Dietzschold et al., 2000; Morimoto et al., 1996) , potentially facilitating more effective local replication in the dermis, even after a seemingly superficial bite by this bat species. This type of situation, where a species has evolved genetic changes associated with enhanced viral infectivity, has been described as the increased infectivity hypothesis (Messenger et al., 2003a) , although currently this theory remains largely unproven . Between EBLVs, a difference in pathogenicity is believed to occur, with EBLV-1 being potentially more virulent than EBLV-2, with all reported spillover infections in terrestrial (non-human) mammals being of EBLV-1 origin. Recent studies have indicated that foxes (Vos et al., 2004a) , cats, mice and ferrets are more susceptible to EBLV-1 infection than EBLV-2, (Vos et al., 2004b) , as is also the case in murine models (Brookes et al., 2005a,b) . No spillover hosts have been reported for ABLV; recorded human infections have been caused by direct exposure to infected bats (Mackenzie et al., 2003) . ABLV infection has not been identified in either domestic or wild (non-bat) mammal species (McColl et al., 2000; Mackenzie et al., 2003) , suggesting that the virus cycles only in bats. ABLV susceptibility studies have initially found that both cats and dogs infected experimentally do seroconvert, and in some cases, exhibit clinical signs (Mackenzie et al., 2003) . In the final part of this review, we discuss the effects of rabies control measures on bat populations, with both positive and negative outcomes, in relation to biodiversity and conservation. The importance of education and awareness is discussed, especially regarding current policy and advice for bat research workers. There is sparse evidence for accurate assessment of the impact of rabies on bat populations. Knowledge of EBLV epidemiology and prevalence is limited. Few large-scale die-offs of bats have been reported (CDC, 1964; Clark et al., 1996) , and rabies was not officially confirmed as the primary cause of death in these (Constantine, 1967a,b) . Difficulty in quantifying die-offs may come from a lack of knowledge of baseline population size and mortality rates in wild animals. Adequate knowledge of the behavioural ecology of any rabies vector species, especially those such as bats, as endangered and/or protected species, is integral to the successful management of rabies (Macdonald, 1993) . This highlights the need for increased research into the epidemiology of bat rabies, and population studies of potential or known host species, combined with an increase in surveillance. Rabies control measures and associated management strategies for bats remain limited, partly due to the high mobility of bats. Management is frequently aimed at public awareness and habitat modification, such as the exclusion of bats from a particular building (Frantz and Trimarchi, 1983; Greenhall, 1982) . This however, can be difficult to achieve, and unnecessary if contact can be minimised by other means. A study in Spain identified an antibody prevalence to EBLV-1 of 7.8% (Serra-Cobo et al., 2002) in bat colonies in areas frequently visited by members of the public. The entrances to the caves in which the colonies live are now grilled, human access is controlled and limited during periods of bat habitation. In Latin America, an estimated 0.15% of 70 million cattle are lost each year due to vampire bat-related rabies, costing the economy $US30 million dollars per year (Acha and Arambulo, 1985) . Vampire bat control programmes have produced ill-conceived and indiscriminate methods for reducing populations (Acha and Arambulo, 1985; Greenhall and Schmidt, 1988) , with techniques such as firearms, electrocution, smoke, flame-throwers, dynamite, poison gas, and Newcastle disease as atomised virus used to destroy individuals and roosts (Hutson et al., 2001) . These methods may produce short-term reductions in the prevalence of rabies in cattle, but risk the geographical dispersal of disease through forcing bats to move from disrupted roosts into areas where perhaps rabies was not previously a problem (Fooks, 2004d) . Bat Conservation International (BCI) has implemented education programmes regarding management of vampire bat populations, in an attempt to promote efficient, species-specific control (Lord, 1988) . Experimental RABV vaccination of a captive vampire bat species (D. rotundus) indicated that oral vaccination methods (more suited to potential field vaccination programmes) produce lower rates of sero-conversion than intra-muscular (IM) routes (Aguilar-Setien et al., 1998 . In Europe, alternative management strategies, such as vaccination against rabies of domestic dogs in Denmark (Fedaku et al., 1988; Racey, 1992) should be viewed as positive conservation efforts, taking into consideration both bat conservation and human health, protecting bat populations whilst protecting people. The current risk of EBLV spill-over from bats to other organisms in Europe is believed to be low, in comparison with RABV spill-over in both North and Latin America, where outbreaks of bat variant RABV have been reported in striped skunks (Mephitis mephitis) in Arizona (Smith et al., 2001) and detected (by monoclonal antibody screening) in other mammal species such as cats, dogs, cattle, horses, sheep and foxes (Messenger et al., 2003a) . Control methods such as those used for vampire bats may have impact on other non-target bat species (Hutson et al., 2001) , and in turn affect biodiversity at a local, if not wider scale. In Venezuela, from 1964 to 1966, an estimated 900,000 bats of various species were gassed annually as part of vampire bat control programmes. Losses of non-target bat species are also thought to have occurred due to the barricading of caves (Pint, 1994) , selective burning of trees, and application of anti-coagulent paste (McCarthy, 1978) on randomly caught bats. The potentially detrimental effect of actions such as these upon the local ecosystem, and the effect on bat species diversity have not yet been studied in detail (Hutson et al., 2001) . The control of vampire bat populations, in relation to the protection of domestic livestock and humans, may be necessary in certain geographic regions. However, the main aims of any control strategy should be first, to regulate the population levels of the target species (rather than indiscriminate destruction of individuals) and second, to ensure protection of non-target species, to maintain species diversity (Greenhall, 1968; Lord, 1988) . Attitudes and education: conservationists and the general public The conservation of bats in certain areas of the world has been significantly affected by human perception of their potential as vectors and transmitters of lyssavirus (McCracken and Rupprecht, 2004; Mickleburgh et al., 1992 Mickleburgh et al., , 2002 Temby, 2004) . This, in turn, may result in habitat and/or roost loss, due to reduced tolerance of bats in proximity to human dwellings. Occupational exposure is a potential risk, for groups such as bat researchers, bat care workers/rehabilitators, builders, fishermen, arborists and vets. Education efforts reflecting scientific advice regarding the human health risks associated with bat rabies are essential. Risks to the general public remain minimal, but the fatal consequences of rabies mean that the hazard must be taken seriously. Continuity across countries, regarding handling methods (gloves), vaccination (compulsory or highly recommended) and treatment after potential exposure, are all integral in creating a Europe-wide agreement on management and conservation of bat populations (Racey and Fooks, 2005) . Prophylactic vaccination is recommended for those professionally or recreationally exposed to bats in most European countries. Within the UK, there are a number of organisations concerned with bat conservation (e.g. BCT, Mammals Trust UK, Mammal Society, Scottish Natural Heritage (SNH)), that now have the additional role of advising their members and the general public on bat lyssaviruses issues. During the past 15 years, the number of confirmed cases (virus positive) of EBLV in Europe has increased in direct association with an increase in surveillance. Bat-associated rabies cases are likely to be under-estimated globally due to lack of reporting or recording of bat related occurrence and/or the lack of rabies isolate typing. The EBLV-2 lyssavirus strain is thought to have been present in the UK for a considerable time (Racey and Fooks, 2005) , but the potential spread and infection within bat populations, and the perceived health risk to humans are newer, more immediate issues, requiring surveillance, research and education to enable bat conservation to continue worldwide in a realistic and informed manner. Surveillance programmes for EBLVs throughout Europe and the UK play an integral role in developing a greater understanding of both the transmission and prevalence of the disease. Integrated with this should be research on bat behaviour and movement patterns, to enable the relationship between disease and host to be fully understood. Rabies in the tropics -history and current status Experimental rabies infection and oral vaccination in vampire bats (Desmodus rotundus) Vaccination of vampire bats using recombinant vaccinia-rabies virus Salivary excretion of rabies virus by healthy vampire bats A human case of encephalitis due to lyssavirus recently identified in fruit bats Evolution of European bat lyssavirus Animal Health in Australia New lyssavirus genotype from the Lesser Mouse-eared Bat (Myotis blythi) Serologic evidence of lyssavirus infections among bats, the Philippines Rabies in individual countries France (3.13). Rabies Bulletin Europe 99/2, 6 The spread and present occurrence of the Serotine (Eptesicus serotinus) in Denmark Eptesicus serotinus (Schreber, 1774) -Breitflugelfledermaus Evidence of two lyssavirus phylogroups with distinct pathogenicity and immunogenicity Rabies in non-haematophagous bats Australian bat lyssavirus: observations of natural and experimental infection in bats Report of isolations of unusual lyssaviruses (rabies and Mokola virus) identified retrospectively from Zimbabwe Novel lyssaviruses isolated from bats in Russia New human rabies case from a bat in Ukraine Isolation of a virus from Nigerian fruit bats Antigenic and molecular characterisation of bat rabies virus in Europe Molecular diversity of the Lyssavirus genus Ecology and evolution of rabies virus in Europe Natural History and Public Health Implications European bat lyssavirus in Scottish bats Rabies human diploid cell vaccine elicits cross-neutralising and cross-protecting immune responses against European and Australian bat lyssaviruses Behavioural observations in some rabid bats Outbreak of vampire bat biting in a Venezuelan village Centre for Disease Control and Prevention (CDC), 1964. Rabies in bats -Mississippi. Veterinary Public Health Notes The epidemiology of bat rabies in Dead and dying Brazilian free-tailed bats (Tadarida brasiliensis) from Texas: rabies and pesticide exposure Rabies and rabies-related viruses: a modern perspective on an ancient disease. Revue scientifique et technique de l office international des epizooties 23 Susceptibility of flamingos to cyanobacterial toxins via feeding Rabies transmission by the non-bite route University of New Mexico Publications in Biology Rabies transmission by air in bat caves. US Public Health Service Publication 1617 Ecological and Behavioural Methods for the Study of Bats Transmission of pathogenic microorganisms by vampire bats Cluster of rabies cases of probable bat origin among red foxes in Prince Edward Island Viral encephalitis in England, 1989-1998: what did we miss? The fluorescent antibody test Genotypic and phenotypic diversity of rabies virus variants involved in human rabies: implications for postexposure prophylaxis Illustrated Identification Key to the Bats of Europe. Version 1.0, released 15/12/2004 -electronic publication Screening of active lyssavirus infection in wild bat populations by viral RNA detection on oropharyngeal swabs Parties and Range States to Eurobats European bat lyssavirus: an emerging zoonosis Case report: isolation of a European bat lyssavirus type-2a from a fatal human case of rabies encephalitis Detection of antibodies to European bat lyssavirus type-2 in Daubenton's bats in the UK. The Veterinary Record Identification of a European bat lyssavirus type-2 in a Daubenton's bat found in Staines, Surrey, UK. The Veterinary Record Identification of a European bat lyssavirus type-2 in a Daubenton's bat found in Lancashire The challenge of emerging lyssaviruses Bats in human dwellings: health concerns and management Encephalitis caused by a lyssavirus in fruit bats in Australia Cryptogenic rabies, bats, and the question of aerosol transmission A characterisation of a novel lyssavirus isolated from a pteropodid bat in Australia Bat rabies in Denmark Bats, rabies and control problems House bat management Natural History of Vampire Bats Australian bat lyssavirus infection: a second human case, with a long incubation period Passive surveillance for European Bat Lyssaviruses in UK bats 1987-2004. The Veterinary Record A Review of British Mammals: Population Estimates and Conservation Status of British Mammals Other Than Cetaceans. JNCC Heminested PCR assay for detection of six genotypes of rabies and rabies-related viruses Cases of rabies in Germany following organ transplantation Isolation of Listeria monocytogenes in slaughter animals and bats of Togo (West Africa) A new lyssavirus, the first endemic rabies-related virus recognised in Australia Histopathology and immunohistochemistry of bats infected by Australian bat lyssavirus Human-to-human transmission of rabies virus by corneal transplant Evolutionary timescale of rabies virus adaptation to North American bats inferred from the substitution rate of the nucleoprotein gene Serotine Eptesicus serotinus Microchiropteran Bats: Global Status Survey and Conservation Action Plan. IUCN/SSC Chiroptera Specialist Group Occurrence, distribution and incidence of Lyssavirus in bats Human rabies and bat bites. The Lancet 357, 1714. Joint Nature Conservation Committee (JNCC) Phylogenetic comparison of the genus lyssavirus using distal coding sequences of the glycoprotein and nucleoprotein genes Isolation of a European bat lyssavirus type-2 from a Daubenton's bat in the United Kingdom Airborne transmission of Lyssaviruses European bat lyssavirus type 2 RNA in Myotis daubentonii Diagnosis of rabies by polymerase chain reaction with nested primers Bat Rabies Surveillance in Europe Fission, fusion and nonrandom associations in female Bechstein's bats (Myotis bechsteinii) Lyssavirus infections in European bats The mouse inoculation test Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P and G gene sequences Phylogenetic relationships within the Lyssavirus genus and suggested quantitative criteria based on the N gene sequence for lyssavirus genotype definition Veterinary Nursing Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats Fruit bats as reservoirs of Ebola virus Bats are natural reservoirs of SARS-like coronaviruses Action Plan for the Conservation of the Pond Bat in Europe (Myotis dasycneme). Council of Europe Publishing Control of vampire bats Human rabies of bat origin in Europe Survey for bat Lyssaviruses Rabies and wildlife: a conservation problem? Managing emerging diseases borne by fruit bats (flying foxes), with particular reference to henipaviruses and Australian bat lyssavirus First case of bat rabies in the Czech Republic Comments on paralytic rabies in Belize. Contribution of the Vampire Bat Education and Control Program Human depredation by vampire bats Desmodus rotundus following a hog cholera campaign Bat lyssavirus infections. Revue scientifique et technique de l'office international des epizooties 19 Implications of rabies for bat conservation efforts An unusual case of human rabies thought to be of chiropteran origin Emerging epidemiology of bat-associated cryptic cases of rabies in humans in the United States Emerging pattern of rabies deaths and increased viral infectivity Bats, emerging virus infections, and the rabies paradigm Old World Fruit Bats. An Action Plan for their Conservation A review of the global conservation status of bats Rabies, Humans, Vampire bats -Brazil. A Pro-med Article Bat Workers' Manual. JNCC, Peterborough. pp. 178. Morbidity and Mortality Weekly Report (MMWR), 1986. International Notes Bat Rabies -Europe Characterisation of a unique variant of bat rabies virus responsible for newly emerging human cases in North America Review of reported rabies case data in Europe to the WHO collaborating centre Tü bingen from 1977 to Infection of a stone marten with European bat lyssavirus (EBL1) Rabies-free -as understood by WHO and OIE Spill-over of European bat lyssavirus type 1 into a stone marten Journal of Veterinary Medicine Series B -Infectious Diseases and Veterinary Public Health Fatal human rabies caused by european bat lyssavirus type 2a infection in Scotland Isolation of rabies virus from brain, salivary and interscapular glands, heart, lungs and testis of the bat Desmodus rotundus, in the State of Sao Paulo (author's translation) Epidemiology of human rabies in the United States Ability of rabies vaccine strains to elicit cross-neutralising antibodies Do bats acquire immunity to rabies? Evidence from the field Serological status of bats in relation to rabies: What does the presence of anti-rabies virus neutralizing antibodies mean? Rabies in the vampire bat of Trinidad, with special reference to the clinical course and the latency of infection The transmission of paralytic rabies in Trinidad by the vampire bat (Desmodus rotundus murinus, Wagner 1804) Lyssavirus in Eptesicus serotinus (Chiroptera: Vespertilionidae) Genetic analysis of European bat lyssavirus type 1 isolates from France Epidemiology of rabid bats in France Who cares about Mexican bats? Rabies surveillance in Europe Bat rabies in the Union of Soviet Socialist Republics Other animal species, accumulated totals. Rabies Bulletin Europe (25/4), 9. Rabies Bulletin Europe The conservation of bats in Europe Rabies in bats in Britain Angiostrongylus cantonesis Infection in Grey-headed Fruit Bats Anti-brucella agglutinins in bats and Callithrix monkeys Rabies, Humans, Vampire Bats -Peru. A Pro-Med Article Myotis dasycneme (Boie, 1825) -Teichfledermaus Myotis daubentonii (Leisler, 1819) -Wasserfledermaus Fatal encephalitis caused by a bat-borne rabies-related virus; clinical findings Clinically silent rabies infection in (zoo) bats. The Veterinary Record A new case of European bat lyssavirus (EBLV) infection in Danish sheep Non-rabies lyssavirus human encephalitis from fruit bats: Australian bat lyssavirus (pteropid lyssavirus) infection Rabies in bats in Florida Expert Consultation on the Care of Persons Exposed to Rabies Transmitted by Vampire Bats. PAHO/WHO. Programs for Veterinary Public Health Potential force of infection of human rabies transmitted by vampire bats in the Amazonian region of Brazil Ecology and epidemiology of attacks upon humans by the common vampire bat Rabies-related Yuli virus; identification with a panel of monoclonal antibodies European bat lyssavirus infection in Spanish bat populations Rabies in a colony of big brown bats (Eptesicus fuscus) African viruses serologically and morphologically related to rabies virus An Eocene big bang for bats Order Chiroptera Studies on the pathogenesis of rabies in insectivorous bats -3. Influence of the gravid state Lyssaviral infection and lead poisoning in black flying foxes from Queensland Molecular epidemiology of rabies in the United States Molecular evidence for sustained transmission of bat variant of rabies virus in skunks in Arizona Bat rabies in the United Kingdom Reactivation of rabies virus infection in a guinea pig with adrenocorticotropic hormone Reactivation of rabies virus in a guinea pig due to the stress of over-crowding Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp Transmission of rabies virus from an organ donor to four transplant recipients Distribution and status of bats in Europe Serotine bat behaviour in Great Britain. Final Report for the Ministry of Agriculture Fisheries and Food Rabies in individual countries: Denmark Migratory and stationary bats (Chiroptera) of the European part of the Soviet Union Studies on the pathogenesis of rabies in insectivorous bats -1. Role of brown adipose tissue Studies on the pathogenesis of rabies in insectivorous bat -2. Influence of environmental temperature Lead poisoning in grey-headed fruit bats Experimental inoculation of plants and animals with Ebola virus A molecular phylogeny for bats illuminates biogeography and the fossil record Urban wildlife issues in Australia Health and conservation implications of Australian bat lyssavirus Antibodies to EBLV-1 in a domestic cat in Denmark Natural and experimental infection of sheep with European bat lyssavirus type-1 of Danish bat origin Naturally occurring rabies virus and neutralising antibody in two species of insectivorous bats of New York State New York State Rabies Annual Summary Rabies in the insectivorous bat Tadarida brasiliensis in southeastern Brazil Bats as vectors of rabies Characterisation of a recently isolated lyssavirus in frugivorous zoo bats European Bat Lyssaviruses, the Netherlands. Emerging Infectious Diseases 11 Susceptibility of ferrets (Mustela putorius furo) to experimentally induced rabies with European Bat Lyssavirus (EBLV) Rabies in red foxes (Vulpes vulpes) experimentally infected with European Bat Lyssavirus Type 1 Rabies and other lyssavirus diseases Public health surveillance for Australian Bat Lyssavirus Virus isolation in neuroblastoma cell culture Presence of European bat lyssavirus RNAs in apparently healthy Rousettus aegyptiacus bats First isolation of a rabies-related virus from a Daubenton's bat in the United Kingdom Airborne rabies transmission in a laboratory worker World Health Organisation (WHO) 2006. Human and Animal Rabies Survey of rabies among free-flying bats from the Big Bend region of Texas The lyssavirus research and surveillance studies in British bats are funded by the UK Department for Environment, Food and Rural Affairs (Defra ROAMEs SEO418, SV3026, SV3027, SV3500). S.H. was funded by a BBSRC studentship and by financial support from the VLA (Seedcorn Grant SC0149).