AUTHORS: D. Lichawsky*, S. Perl**, B. Yakobson**, & U. Orgad**
*. Koret School of Veterinary Medicine, P. O. Box 12, 76100 Rehovot,
**. Kimron Veterinary Institute, P. O. Box 12, 50250 Beit Dagan
In 1953 rabies was first diagnosed in bats in the USA. Since then several surveys were conducted to detect the prevalence of the virus in the bat populations. This is between 0.5% and 4.6%. The species most infected in the New York State survey was E. fuscus with 90% affected. A similar if not identical species, E. serotinus, which lives in Europe was found to be the most infected bat with an 87% infection rate. Rabid bats have been found in England, considered a rabies-free country; the bats probably came from France by flying across the British Channel. Rabid bats were never detected in Israel but the number of bats tested is very low. Most are fruit bats but none belonged to E. serotinus spp. (1,2). In light of the isolation of PBV in Australia from fruit bats further studies should be made in order to gain more knowledge of potential zoonotic viruses in bat populations.
Introduction -The bat species
Bats are among the largest and commonest groups of mammals. There about 980 different species and are found worldwide, except for the polar regions. Bats are considered to be the only true flying mammal and because of their unique nocturnal flight activities they have a special ecological niche. Bats belong to the order Chiroptera (hand wing) which has two sub-orders: Megachiroptera and Microchiroptera.
The Megachiroptera include the Pteropodidae. These are the fruit bats of the old world and are known as the flying foxes. This sub-order is common in tropical and sub-tropical zones and of the 175 known species only one is indigenous to Israel.
Sub-order Microchiroptera includes 4 super-families:
1. Emballonuroidea, 2. Rhinolophoidea, 3. Phyllostomoidea with the subfamily Desmonontinae including three species of blood-sucking bats which are found in south and central America (3) and 4. Vespertilinoideawith the subfamily Eptesicus; Eptesicus serotinus resides in Europe and Asia while Eptesicus fuscus is found in New York State. Both of these carry rabies virus more frequently than other bats. Whether these are one or two separate species is still being debated (4,5,6).
Bats in Israel
In Israel there is only one species of fruit bat, belonging to the Megachiroptera sub-type. Rousettas aegypticus is common in northern and central Israel where they live all year round. There are 31 species belonging to the Microchiroptera in Israel and these belong to 18 families. Being insectivorous bats their diet consists of insects. Insectivorous bats are decreasing in numbers in Europe, USA and Asia mainly due to their sensitivity to insect repellents and reduction in the number of roosts. The end result is a reduced birth rate. Information on their populations in Israel and the neighboring countries is very limited.
The following bats are more frequent in Israel. Data on their geographical location and roosting habitats are given (7,8).
Rhinolophidae family (8). Rhinopoma micropjyllum, heir habitat in dry caves and cliffs seen along entire length of Syrian-African Fault in the Galilee, Yehuda, Shomron and Carmel districts. They are seen all year round and it is likely that they are active in several areas. Rhinopoma hardwickei lives in cliffs and in caves along the Syrian-African Rift, the Galilee and Yehuda hills. Molossidae family. Tadarida teniotis lives in cliffs, caves and tall buildings with an ability to adapt to different habitats. Common throughout the country and can move about.
Vespertilionidae family, most of the group is feared to be extinct.
Two members are associated with rabies virus: Eptesicus serotinus, which is found in cliffs, in caves and sometimes in trees. In Europe it is found near populated areas; and in Israel is found in the Galilee and the Golan. World-wide it is found in Europe, North America, and as far as China to the east. There are fast growing populations in Scandinavia. A good example is Denmark, where until 100 years ago they were not found, but today their growing numbers have become a pest to the local residents (7,8). Eptesicus fuscus inhabits the US, Eptesicus serotinus is probably present in Israel (5)
Rabies in bats
Bats are known to be carriers of rabies mainly in the Americas (first cases reported in 1953) and rarely in Europe and Asia. Of the 9 species found in the US, six are reported as being infected more than once.
The level of the rabies virus among bats is unknown due to lack of controlled studies. In a survey on asymptomatic bats, conducted in the US, 0.5% were found to be affected. On the other hand in another study performed on thousands of bats, in New York State in the 1980’s, 4.6% were found to be rabies positive. In this study both non-symptomatic bats with non- specific signs such as cachexia and weakness were included. Of the rabid bats in the New York study 90% were Eptesicus fuscus. In Europe, where over the past 20 years there has been an increase in rabies cases, Eptesicus serotinus was found to be mostly affected and in a survey conducted between 1954 and 1989, out of 379 rabies positive bats, 331 (87%) were E. serotinus species (4,5,9,10).
In rabid bats clinical signs include loss of appetite, progressing to paralysis and death. The rabid bat become a loner in its colony; is thin, cachectic, dehydrated, weak, paralyzed and at times, hypothermic. The majority of bats do not show aggressive signs of the disease except for flying attempts that result in falling to the ground or by finding it on the ground during the daytime. There are different clinical signs of the disease among the rabid bats living in colonies and in solitary rabid bats which more usually show the aggressive nature of the disease(2,9).
Transmission of the virus occurs usually by biting and that is also true for bats. The virus is transmitted in bat populations through mutual biting - the normal social behavior of bats.
Aerosol transmission of rabies was confirmed on two different occasions to two affected persons who entered the Frio caves in Texas. Transmission by ingestion was experimentally demonstrated in skunks, when 6 out of 18 that ingested a rabid bat carcass developed rabies. In another study on cats that ingested rabid mice, none became ill and the virus was not isolated from their saliva (9).
The incubation period of rabies in bats is normally no different from that in other warm-blooded animals, whereas the reduced metabolic rate in hibernating bats can lengthen the incubation period. The longest incubation period reported was in Eptesicus fuscus, which developed signs of the disease 204 days after capture and died four days later. The presence of virus in saliva before signs of the disease appear resembles rabies in other mammals. The longest time of the virus in saliva was 12 days in two insectivorous bats Tadarida brasiliensis. Bats, including vampire bats are not asymptomatic carriers of rabies; but show signs andsymptoms like any other mammal. It seems that this misconception is due to other viruses that can chronically infect their salivary gland – such as the Rio Bravo virus and the Tamana bat virus. (3,9,11).
Rabies-related viruses in bats
The importance of these viruses became evident when they were discovered among bats thought to be rabid, and were isolated from insectivorous, fruit and vampire bats.
In this paper we will mention only two: Duvanhage virus, first isolated in 1970 from an adult male who died from a rabies-like disease, five weeks after being bitten by an insectivorous bat. Since then a few more human cases have been recorded and all had previous contact with bats(11). In a survey conducted in Europe in 1985, there were approximately 450 isolations of the Duvanhage virus, and the majority were from asymptomatic bats. Since 1985, there are over 40 cases of rabid bats yearly infected with Duvanhage virus(11). Pteroid Bat Virus (PBV) was first isolated in Australia in 1996 from a fruit bat that showed signs of paralysis, was unable to fly and exhibited a mild tremor. On histopathological examination viral encephalitis was present and consistent with the clinical signs.
Immunoperoxidase testing was positive for a Lyssavirus. Electromicroscopy showed bullet- shaped particles that strongly indicated that rabies or a rabies-like virus was involved. PBV virus was shown to be closely related to rabies virus by PCR. In November 1996, a woman who was a bat handler became ill with numbness and weakness in her left arm, she progressed into coma and death from encephalitis 20 days after being diagnosed as infected with PBV by PCR analysis of her CSF and specific neutralizing antibody to rabies virus was demonstrated in her serum. She had never been vaccinated against rabies. PBV has only been reported in Australia (12).
In 1966, Akov and Goldwasser reported on the prevalence of antibodies to T.M.E (Turkey meningoencephalitis) and West nile viruses in fruit bats in Israel (13). No further attempts to study this matter have been reported.
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2. Lubinsky, D.: The presence of rabies virus in the common fruit bat. D.V.M. thesis 1997. (In Hebrew).
3. Tuttle, M.: Introduction to the natural history of vampire bats. In: Arthur, M. (ed.), Natural History of Vampire Bats. CRC press. Bocca Raton, Florida, 1988.
4. Barrot, J.: Two bats diagnosed rabid in France. Rabies bulletin Europe 10-11, 1989.
5. Child, J.E.: The epidemiology of bat rabies in New York State. 1988-92. Epidemio. Infec. 113: 501-511, 1994.
6. Hill, J.: Bats: A natural History. James, D. (ed.) University of Texas Press, Austin. pp. 186-221, 1984.
7. Makin, D.: The status of bats in Israel. European bat research. Charles Univ. Press, Praha pp. 403-408, 1987.
8. Ron, T.: Plans for the assessment and protection of Insect Bats in Israel. Natural Conservation Council, June 1-5, 1995. (In Hebrew).
9. Constantine, D.: Biology of bats. Volume 2 William, A. (ed.) pp. 328-414, 1970.
10. Coulow, P.: Rabies virus antigenicity. An overview. Onderstepoort J. Vet. Res. 60: 271-275, 1993.
11. Warepoel, B.: Rabies-related virus In: King, A.: Int. congress on epidemiology, control and prevention of rabies in eastern and southern Africa. Zaire, June 1-5, 1992. Pp.69-72.
12. Muller, W.: New Lyssa virus in fruit bat in Australia. Rabies Bulletin Europe 9-10, 1996.
13. Akov, Y. and Goldwaser, R.: Prevalence of antibodies to artboviruses in various animals in Israel. Bull. WHO 34: 901-909, 1966.