Health and conservation implications of Australian bat Lyssavirus Christopher R. Tidemann,' Michael J. Vardon,'a2 John E. Nelson,' Richard Speare4 and Laurence J. Gleeson5 'School of Resource Management and Environmental Science, Australian National University, Canberra, Australian Capital Territory 0200 'Wildlife Management International Pty I.td, P.O. Box 530, Sanderson, Northern Territory 0812 'Department of Ecology and Evolutionary Biology, Monash University, Clayton, Victoria 3168 'Department of Public Health and Tropical Medicine, James Cook University, Townsville, Queensland 481 1 'CSIRO, Australian Animal Health Laboratory, Private Bag 24, Geelong, Victoria 3213 ABSTRACT Australian bat Lyssavirus, first reported in mid-1996 from a Black Flying Fox Reropus alecto has now been isolated from two other species of flying fox, a microbat and a human, who died of a rabies-like illness. Infected animals have been identified from widely separated localities in four Australian states. It is not known definitely from which species of animal the human victim contracted the disease, which is (are) responsible for spreading it. nor whether it is an old disease or one that has recently entered Australia. The infectivity of Australian bat Lyssavirus to humans and other mammals is not known, but its close genomic and antigenic relationship to classical rabies virus suggest that it is likely to be capable of causing fatal illness in most mammalian species. Its similarity to classical rabies virus also indicates that humans and other mammals will be protected by existing rabies vaccines. The discovery of Lyssavirus in Australian bats has highlighted the need for professional and community groups involved with wild animals to work together to decrease the risks to human health and to lessen the impact on bats and other native species. Educating the public about the risks of contact with bats is the single most important safeguard in protecting humans from a bat-borne disease. Concurrently, people need to be informed of the important role of bats in maintaining biodiversity and ecosystem integrity to minimize public impact on bats. OVERVIEW OF LYSSAVIRUSES jackals, mongooses, primates, raccoons, raccoon dogs, skunks and shrews (Constantine 1988; The best known of the lyssaviruses is that Brass 1994; Fishbein and Bernard 1995; Krebs which causes classical rabies, one of the most et al. 1995) can also contract or transmit rabies feared and respected of the zoonoses - animal to humans or other species. pathogens that affect humans (Kunz et al. 1996). Classical rabies has been known from the Middle Classical rabies virus is one of a group of East since before 2 300 BC, and is now known closely related viruses in the genus Lyssauirus in to occur on every continent, except Australia the family Rhabdoviridae; other species known and Antarctica (Brass 1994; Fishbein and prior to 1996 were: Lagos bat; Mokola; Bernard 1995). Worldwide an estimated Duvenhage and European bat 1 and 2 (Krebs et 40 000-100 000 human deaths are caused by al. 1995; Rupprecht et al. 1995). All but Lagos classical rabies virus each year, mostly from dog bat virus are known to have caused rabies-like bites (>go%) and mostly in developing countries illness and deaths in humans (Brass 1994; (99%), where health care is minimal (Smith and Fishbein and Bernard 1995; Krebs et al. 1995). Seidel 1993; Brass 1994; Fishbein and Bernard Few fatalities have been documented, but this 1995; Rupprecht el al. 1995). Only a few may be in part because the disease cannot be humans die of rabies in the US each year, but distinguished from classical rabies unless the annual cost of prevention of the disease is modern diagnostic tests are applied. In Africa estimated to be in the region of US$300 million, and Asia it seems almost certain that much most of which is spent on animal vaccination information about non-classical rabies lyssa- (Smith and Seidel 1993; Rupprecht et al. 1995), viruses is masked by the almost ubiquitous with US$45 million being spent on human presence of classical rabies (Aghomo et al. 1990; vaccination (Anon. 1995b). Blood-feeding Rupprecht et al. 1995). In Europe the existence Vampire Bats Desmodus rotundus cause serious of two variants of bat-borne Lyssauirus was not outbreaks of human rabies in South and Central recognized until very recently (Baer and Smith America (e.g., Lopez et al. 1992) and the annual 1991). cost to the cattle industry is immense, although difficult to calculate because of unco-ordinated Non-rabies lyssaviruses are found in various reporting (Brass 1994). Many other mammals, species of mammal, particularly bats (Brass including bats, cat, coyotes, ferrets, foxes, 1994; Rupprecht et al. 1995). Lagos bat virus March 1997 Australian Zoologist 30(3) 369 Q/) \d s\ aq 0 (Y \rAs1 Figure 1. Location of bats found infected with Australian bat Lyssaoirus (solid circles) and other localitiesm entioned in text. has been identified in African fruit bats (Eidolon 1996). It has now been isolated from other P. heluum, Micropteropus pusillus, Epomorphorus alecto, frorn Little Red Flying Foxes P. scapulatus, wahlbergi), dogs and cats. It is the only one of the Grey-headed Flying Foxes P. poliocephalus and a group that is not known to have caused human Yellow-bellied Sheathtail Bat Saccolaimus death, but this could be because of confusion f.a,aiaentris from widely separated locations on with classical rabies. Mokola virus has been the continent (Fig. t). The Lyssaairusi solated in identified in African shrews (Crocidura spp.) Australia is a new serotype (Fraser et al. 1996b; and rodents (Lophuromys sikapus and Tatera Lyssavirus Expert Group 1996; Gleeson 1997), leucogaster)a, nd dogs and cats. Duvenhage virus but fortunately the treatments and vaccines has been found in African Slit-nosed Bats developed for classical rabies give effective Nycteris thebaica and unidentified insectivores. It protection (Lyssavirus Expert Group 1996). has not been identified in domestic animals. The They offer only marginal protection from Lagos European bat lyssaviruses have been found in bat, Duvenhage and European bat virus I and many species of microbat, particularly Eptesicus 2 and no protection from Mokola virus serotinw and Myotis spp., and, although human (Rupprecht et al. 1995). At this stage the infec- deaths have occurred. neither is known to infect tivity of Australian bat Lyssauirus to domestic dogs or cats. animals and other wildlife is unknown. Its close Australian bat Lyssaairus was first isolated in genomic and antigenic relationship to classical May 1996 from a juvenile Black Flying Fox rabies virus suggest that it would be capable of Pterops alecto from northern New South Wales causing fatal illness in humans and most other (Fraser et al. 1996 a,b) and in November of the mammals (Fraser et al. 1996; Gleeson 1997). same year it caused a human fatality in an Information about the geographic distribution animal handler from central Queensland of bat families with classical rabies and other (Allworth et al. 1996; Lyssavirus Expert Group lyssavirusesi s summarized in Table l. 370 AustralianZ oologist3 0(3) March 1997 Table 1. World distribuuon of families of ham reported with rabies and other lyssaviruses. Drawn from Consrantine (1988): Brass (1994): Rupprecht d 01. (1995). Family America Eumpe Aria Africa Austmlia Pteropodidae - - +(*I +(**I +(**I Emballonuridae +(*I - + + +('*) Nycteridae - - + +(**I - + + + Rhinolophidae - +(*I Noctilionidae +(*I - - - - Mormwpidae +(*I - - - - Phyllostomidae +(*) - - - - + + + Vesperulionidae +(*) +(*,**I + + + + Molossidae +(*) +family occurs on landmass. *classical rabies. **no"-rabies Lpvirur DISEASE CAUSED BY LYSSAVIRUSES 1995; Krebset al. 1995). In 95% of human rabies IN HUMANS AND DOMESTIC ANIMALS cases svm~tomsd evelov within one vear of exposu;e i~ishbeina nd Bernard 1995). The Infection with classical rabies and the other course of the disease caused by the other lyssaviruses is usually spread by the bites of lyssaviruses is similar, although this statement is animals carrying the disease (Brass 1994; based on very few documented cases. Symptoms Fishbein and Bernard 1995). Despite folklore of of rabies in humans are very variable, but can human vampires in some countries (Hand include fever, headache and behavioural 1984), human to human transmission of the changes, including hydrophobia, hallucinations disease is virtually unknown. The virus is shed and paralysis. Once symptoms develop death is in the saliva of infected animals, but can also be almost inevitable (only a handful of cases found in many of the body organs and animals survive) and occurs within a few weeks of their can contract the disease by eating other infected onset (Brass 1994; Fishbein and Bernard 1995; individuals (Afshar 1979). There are four Krebs et al. 1995; Revilia el al. 1995). known cases of human rabies infection by inha- lation of aerosolized virus in confined svaces Most mammals can become infected with with little or no air movement and high concen- rabies, although species vary greatly in their trations of virus, such as bat caves (n = 2) and susceptibility. Some, such as foxes, coyotes, laboratories (n = 2) (Brass 1994). Some species wolves and jackals are highly susceptible, while of animals left in arthropod-proof cages in caves others, such as the American Common Opossum containing rabid bats have also become infected Didelphis marsupialis appear resistant to infection (Constantine 1988). Scratches are capable of (Fishbein and Bernard 1995). Marsupials from resulting in disease transmission if saliva from Papua New Guinea are more prone to experi- an infected animal is also present, but this route mental rabies infections than D. marsupialis of infection is uncommon (Kureishi et al. 1992). (Gerring et al. 1995, pp. 208). Much of the early One case of a person contracting the disease research in this field assumed that rabies was from being licked by a rabid animal has been rabies, irrespective of the animal vector involved recorded (Fishbein and Bernard 1995). Of or the geographic location. The application of particular concern in relation to bat-human modern molecular techniques has shown that interactions is the finding that of the 28 cases of there are many different forms of rabies, each human rabies in the USA since 1980, 15 have associated with a particular primary host species been linked to bat-borne variants of the virus, (reservoir species); many are also restricted to but in only seven cases could contact with a bat particular geographic areas (Baer and Smith be identified. The bites of insectivorous bats are 1991; Smith et al. 1992). In the USA, for relatively small and less likely to be noticed than example, skunk-associated rabies dominates in thosc of'larger animals, hut chis finding s~~ggcsts the central north, whereas in the eastern states that lil~~~ptlc~dy sic;~col ntact uith :a rahid bat m:iv the strain present is hosted primarily by rac- be associated with virus transmission in some coons (Krebs et al. 1995). Rabies of raccoon ori- circumstances (Anon. 1996; Morimoto et al. gin, for example, can be passed to other species, 1996), perhaps lending credence to some of the such as skunks or humans, but in these cases the folklore about the connection between bats and infection is generally a "dead end for both the human illness. virus and the animals to which it is passed. The infectivity and virulence (impact on host) of the In humans the incubation period of rabies different strains vary greatly, depending on the (the time from exposure [=bite] to the first species involved. symptoms) is usually within 30-90 days of the orieinal exoosure. althoueh there are a few cases In the same way, particular strains of bat- on yecord lf peridds exceeYdig six years (Faoagali borne (non-terrestrial) rabies tend to be et al. 1988; Bek et al. 1992; Fishbein and Bernard restricted to particular species of bat. The Australian Zoologist 30(3) 371 reservoir host species of non-terrestrial strains press), although there appears to be no tradi- are hats, although dead-end exposures can tional knowledge of a rabies-like illness follow- occur in many other species, including humans, ing bites (Warner 1937; Berndt and Berndt domestic animals and wildlife (Brass 1994). It is 1989). In Nigeria, where classical rabies and two now possible to determine the particular strain other lyssaviruses are present, the indigenous of rabies involved in a human (or animal) illness people hunt bats in large numbers (Folorunso and, hence, it is possible to reveal a great deal and Okpetu 1975), but they also believe that if of information on the ecology of the disease. a bat bites a person, then madness and death The bat variant responsible for the majority of ensue (Aghomo et al. 1990). Traditional know- recent human cases in the USA circulates ledge of a rabies-like malady is widespread primarily in populations of the Silver-haired Bat among native people throughout the Pacific Zmionyctmi noctivagans although it has recently Northwest (Winkler 1975) and in Central and been isolated from a Red Bat Larium boredis South American countries where vampire-borne that subsequently infected a human (Anon. rabies is prevalent (Brass 1994). One group of 1995). Further work in this area will, no doubt, indigenous South Americans is known to hunt lead to a much deeper understanding of the bats, including Vampire Bats Desmodtu rotundw disease and to improved protection of human (Setz and Sazima 1987). Rabies virus is and animal health (Krebs el al. 1995; Morimoto destroyed by cooking at 54'C for 30 minutes or et al. 1996). 35 seconds at 60% (Fishbein and Bernard 1995) and cases are known of people eating cooked One can expect, therefore, that if Australian rabid dogs with no ill-effect, while individuals bat Lyssavim is an old established disease (see who butchered the carcases contracted rabies Lyssavirus in Australia - whence and when? (Kureishi et al. 1992). There is a clear need for below) and is like its relatives in other countries, the Australia Aboriginal population to be it will probably depend on one or a few species educated about the potential dangers of contact of bat for maintenance and transmission. It is with live or uncooked bats. Since about 3 500 unlikely to establish in populations of terrestrial years BP dingoes have been companions of species, such as dogs and foxes, even though Aboriginal hunters (Corbet 1995) and incidental "dead-end" infections may occur in such species, infection of dingoes from infected bats in other bats and in other species of wildlife. could also pose a health risk in Aboriginal The animal from which the human victim communities. contracted the disease will probably never be known, as the victim was bitten by many Australian fruitgrowers are another group animals, including Common Brushtail Possums that needs to be educated about the dangers of Tvihosurus vulpecula, two species of flying fox bat-borne disease. Many thousands of flying and a microbat. Potential carriers had all been foxes are destroyed annually, usually by euthanased or released before testing could be shooting, on fruit crops on the east coast of done. The molecular evidence, however, Australia (Vardon and Tidemann 1995) and in indicated that the virus responsible for her some areas of the Northern Territory and death probably came from a Black Flying Fox Western Australia (Tidemann, unpubl.; (L. Gleeson, unpubl.). Vardon, unpubl.; Nelson, unpubl.). Dogs are commonly present during "bat-shoots" and foxes in many of these areas scavenge dead and PEOPLE AT RISK AND PREVENTION dying bats. Flying foxes commonly bite fruit OF THE DISEASE other than those they consume (Tidemann and Education of the public about the risks of Nelson 1987). Because the virus is destroyed by contact with bats (and perhaps other wildlife) is exposure to sunlight and drying (Fishbein and the single most important action that can be take Bernard 1995), saliva on the surface of fruit is to minimize the human health risk and the unlikely to remain viable for long. The virus is potentially substantial cost of prevention (Brass also destroyed by acidity (pH of 3 or less), so is 1994; Krebs et al. 1995; Rupprecht et al. 1996). unlikely to survive in the flesh of fruit, which is Children are especially at risk (Kureishi el al. usually acidic (Biale and Young 1981). 1992; Fishbein and Bernard 1995). The current The minimal contact, sometimes with no public view both urban and rural, Aboriginal evidence at all of bites, that is known to result in and non-Aboriginal, that Australian wildlife is human rabies of hat origin in the USA (Anon totally benign needs to be modified to minimize 1996) suggests that any contact between the the risk of people becoming infected with public and bats should be minimized. This Lyssauirus (and probably other zoonoses) would include discouraging people from through contact with infected animals. unnecessarily entering bat caves and preventing Aboriginal people in northern Australia eat contact between bats and humans co-ccupying flying foxes in large numbers (McKnight 1975; buildings (e.g., Tidemann and Flavel 1987). It Altman 1987; Baker 1988; Vardon et al., in suggests also that live bats should not be allowed 372 Australian Zoologist 30(3) to come into contact with the public during, for al. 1995), while two children, one in 1987 and example, educational sessions (Hutson 1996) or another in 1990, contracted the disease while at zoos, unless the animals have been vaccinated travelling overseas, presumably from contact against lyssavirus. with rabid animals (Faoagali et al. 1988; Bek et a/. 1992). Australia is classified as rabies-free People, such as bat researchers or animal (Geering el a[. 1995). rehabilitators, who come into frequent contact with bats (or other possibly infective animals) Australian bat Lyssavirw, first isolated from a should avoid bites and other contact with virus Black Flying Fox, has now been identified in two by wearing protective clothing (Lyssavirus other flying fox species and an insectivorous bat Expert Group 1996). Protective clothing for from widely separated locations in Australia handling large flying foxes should include steel (Fig. 1). All four species have wide distributions mesh gloves (Tidemann and Loughland 1993). (Fig. 2). The current extent of Lyssauirw in People at risk of exposure to Lyssavim should Australia and it origins are, however, unknown also receive pre-exposure vaccination, which (Gleeson 1997). At this stage is seems prudent involves three injections at a total cost of about to assume that it could extend across the whole $AUS300. Immediate washing of bites with continent and could be present in any or all of soap or detergent is recommended if exposure, the '70 or so species of bat that inhabit Australia such as a bite from an infected animal occurs, (Strahan 1995). Strongly colonial species, such followed soon after by post-exposure vaccination as the large flying foxes and some of the cave- (Lyssavirus Expert Group 1996). dwelling microbats may provide populations in which the virus could become amplified, but it Post-exposure treatment is expensive (about is worth noting that the most common strain $AUS800-1,000). Because of the application of causing human rabies in the USA circulates in pre and post-exposure treatment in the USA the Silver-haired Bat Lasionycteris noctzuagan~,a and Europe only a few deaths from rabies are solitary and relatively uncommon species reported each year (Rupprecht el al. 1995), but (Anon.1996). The Yellow-bellied Sheathtail Bat, the cost makes its use prohibitive in many one of the Australian species found infected poorer countries. In the USA the annual bill for with Australian bat Lyssauirm, shares similar human rabies treatment is $US45 million habits (Richards 1995). ($AUS56 million), because infection in a single person can lead to dozens of "exposed people The earliest known case of Australian bat also requiring treatment (Anon. 1995). Recent Lyssauirur is from January 1995 in Townsville, but it is unknown if the disease has been present examples in the USA include 99 people treated in the country for a long time, like the so-called in Arkansas as the result of a single human infec- tion (Gonzales et a/. 1991), 83 in Connecticut equine morbillivirus (= bat paramyxovirus) (Munoz et al. 1996) and 76 in California (Falade (Allworth et al. 1995; Young 1996), or if it is a recent entry. The fact that there is no tradition et al. 1996). Each of these incidents would have among Aboriginal people who have hunted cost more than $AUS70,000 for the vaccine flying foxes for many thousands of years and alone. It is clearly in the public interest to the very large number of non-Aboriginal minimize contact between people and bats in people, particularly in eastern Australia, who Australia, not only because of the health risks, have had close and frequent contact with bats, but also because of the potentially large cost to particularly flying foxes, over the last 20 years, the public purse. There is also a very real risk of suggest either that the disease is a new occur- a public backlash against bats if people are seen rence in Australia or that it is not very infective to contract fatal diseases from them. Only when to humans. But, it is worth noting here that bat- more is known about the infectivity of Australian borne rabies was not identified in the USA until bat Lyssassauirus to people and other mammals will 1953, nor in Europe until 1954 (Rupprechtel al. it be prudent to decrease vigilance. 1995). However, classical rabies is prevalent on both continents and bat-borne occurrences of LYSSAVIRUS IN AUSTRALIA the disease may well have been masked by the -WHENCE ANL) WHEN? much more common source of infection - terrestrial animals. It is possible that Australian Australia, partly because of its relative isolation bat lyssavirus has been present primarily as a and partly because of its quarantine procedures, disease of microbats and has only recently has remained free of rabies and many of the entered the flying fox population through other horrific zoonoses that plague much of the unusual circumstances. Only further testing and rest of the planet. There have been three analysis will provide a definitive answer. recorded human cases of rabies in Australia, but all resulted from the virus entering the country Another possibility is that Australian bat from another landmass. A child in Tasmania is Lyssauim is a recent entry to the continent, in thought to have contracted the disease from a which case one could expect a progressi\rely rabid dog in 1867 (Dunn et al. 1988; Geering et increasing risk of infection to the human Australian Zoologist 30(3) 373 - 'a' V Pteropus alecto Pteropus scqulntus Black Flying Fox Little Red Flying Fox 'd 'd Pteropus poliocephalus Soccolaimuspaviventris Grey-headed Flying Fox Yellow-bellied Sheathtail Bar Figu~e2 . Australian distribution of the four species of bat found infected with Australian bat Lpsmrim. population and to other animals (Gleeson 1997). authorities in developing countries is probably Black Flying Foxes are highly mobile animals substantial. Terrestrial rabies, for example, has and extend beyond the Australian continent to been reported recently in Flores (R.N oske, pers. New Guinea and some of the Indonesian islands comm.) and, considering the existence of several including Sulawesi (Flannery 1990; Kitchener et forms of non-rabies lyssaviruses in Europe and al. 1990; Mickleburgh et 01. 1992; Webb and Africa and now one in Australia, it seems Tidemann 1996). Black Flying Foxes are also probable that bat-borne lyssaviruses are also known to move, on a more or less regular basis, present in South-East Asia. Movements of bats between New Guinea and the islands in Torres within the Australian continent are not well Strait (G. C. Richards, pers. comm.). It is understood. Available information on move- conceivable that the disease could have entered ments of flying foxes (Ratcliffe 1931; Nelson Australia by this route. Little Red Flying Foxes 1965; Eby 1991; Webb and Tidemann 1996) also are highly mobile animals and have been suggests that the patterns are climate-controlled, recorded from southern New Guinea, Ashmore but the domination of the climate of eastern Islands, 350 km to the north-west of Australia Australia by the El Nifio-Southern Oscillation (Fig. 2) and one individual has even reached phenomenon (Nicholls and Kariko 1993) means New Zealand (Sinclair et al. 1996). The Common that the cycles are long-term. Concurrently, the Bent-winged Bat Mintoptem schreibersii, is a rainfall of eastern Australia has increased over species with a world-wide distribution (Dwyer the last 50 years (Nicholls and Lavery 1992). 1995) and some animals may move between Patterns of animal movement controlled by such Australia and neighbouring landmasses. phenomena are not readily elucidated by short- Searches for lyssaviruses in hats on landmasses term studies. adjacent to Australia would enable evaluation of Movement of animals and their diseases can this hypothesis. also be affected by human activities such as Papua New Guinea and Irian Jaya are vegetation clearing and deliberate trans- ostensibly Lyssauim-free, but the potential for locations. The range of the Black Flying Fox has such diseases to go unnoticed by health extended down the east coast of Australia by 374 Australian Zoologist 30(3) March 1997 about 500 km in the last 5 M 0y ears (Webb and assistance over many years and to the following Tidemann 1995), possibly influenced by large- for their help in assembling the information scale changes to vegetation patterns through presented in this paper: David Adams, David clearing (Biodiversity Unit 1995). Deliberate Blair, Chris Bunn, Debbie Claridge, Roger movements of animals by people are also known Coles, Margaret Clunies-Ross, Warren Entsch, to have changed the distribution of diseases; Evelyn Gough, Dinah Hansman, Tony Hutson, movement of asymptomatic but rabid animals Ann Johnson, Bruce Johnson, Shannon Kelson, has changed the epidemiology of rabies in the Monica Jones, Len Martin, Julie Morrison, Ann USA (Krebs et al. 1995; Rupprecht et al. 1995). Munster, Gemma O'Brien, John Padget, Shona A North American bat, Eptesicw fuscus, imported Peters, Bill Rainey, Iris Selby, Sonya Stanvic, Ian into Germany from Canada for scientific study, Temby, Pam Tully, Dianne Vavryn, Josef was found to be rabid (Brass 1994, pp. 276) and Vavryn and Wendy Lees. Ann Biasol, Danny several E. fwcus shipped from the US to Brass, Dan Lunney and three referees provided Denmark for study were subsequently found to very useful comments on earlier drafts of this be infected (Rupprecht et al. 1995). Sasaki et al. paper. 1992 reported a rabid E,f;Sm that was accident- ally transported from continental USA to REFERENCES Hawaii in a shipment of cars. None of these Afrhar. A,, 1979. A review of not-bite transmission of rabies virus latter cases resulted in the establishment of infection. Bnl. Vel. J 135: 14248. rabies, but they illustrate how. t he actions of well Aghamo, H. 0.. Ako-Nai, A. K., Oduye, 0. 0.. 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