Bats as vectors of rabies

South African Journal of Science Vol. 78 October 1982 Vaccinations as well as transmission experiments were conducted on groups of captive kudu. Artificial transmission consisted of collecting saliva from a live. clinically rabid kudu and transferring it mechanically to the macroscopically intact mucous membranes of the lips of healthy susceptible animals. Rabies in the donor animal was diagnosed by the fluorescent antibody test for rabies (FA TR) and the presence of virus in the saliva was also confirmed. Two out of four animals developed clinical rabies (confirmed by FATR), whereas the other two developed humoral antibodies, determined serologically. Thus, transmission via mucous membranes could be successfully achieved. We conclude that circumstantial evidence strongly implicates transmucosal transmission and a horizontal spread of the disease, and hints at a possible role for rabies in controlling animal populations. I. Barnard J.H. and Hassel R.H. (1981). Rabies in kudus. 1. S. Afr. vet. A~. 52, 209-314. 2. Director of Veterinary Services. Department of Ag.riculture and Nature Conservation SW AlNamibia. Annual Reports 1977 - 1981 and naIf-yearly report 1982. 3. Du Pree? J.S. Ecology oftne kudu in SWA. Progress report NO.3. Directorate of Nature Conservation, Windnoek. 4. Griffin M. and Lensing J.E. Biology and ecology of tne kudu: Animal road accident problem in SWA (Final report). Directorate of Nature Conservation. Windnoek. 5. Hassel R.H. Progress report on kudu rabies epizootic 1980. State Veterinarian. Windhoek. 6. Schneider H.P. (1977). AnaIyse der Tiergesundheid Situation in SudwestAfrika/Namibia. Inaugural address. Justus Liebig Universitat. Giessen. 7. Schneider H.P. (1981). Rabies in kudu-antelopes in Soutn West Africa/Namibia. Paper presented at SARCCUS meeting. Pretoria. 8. Shaw J.J.H. (1980). Hondsdolheid by koedoes. 1. S. Afr. vet. Asr. 51.209. Bats as Vectors of Rabies M. van der Merwe Mammal Research Institute, University 0/ Pretoria, Pretoria 0002. In 1972, Geoffrey P. Westl wrote that if a victim could but choose, it would be preferable to be bitten by a rabid vampire bat than by any other rabid animal, since the consequences, though fatal, are then of a less horrifying kind. Unfortunately we do not know much about the symptoms of people bitten by rabid nonhaematophagous bats but, as the rabies carried by insectivorous bats is similar to that transmitted by carniyores,2 it can be expected that the symptoms are similar. Theonly case in South Africa where a person was bitten by a rabid bat supports this assumption.3 It must, however. be stressed that in this case what was involved was a rabies-related virus known as the Duvenhage virus. Vampire bats of the New World are the cause of great concern in Latin American countries; vampire-borne rabies has been declared the primary livestock disease problem and has become a formidable obstacle to the expansion of the agricultural economy.fo About two million animals are lost annually with an associated financial loss exceeding 100 million dollars.5 In this respect, South Africans are fortunate in that vampires do not occur anywhere in Africa. This continent nevertheless is rich in non-haematophagous bat species. Within the borders of South Africa alone, three genera and four species of fruit-eating bats can be found as well as 16 genera and 36 species of insectivorous bats. Many of these species live in close association with man; some species of fruit-eating bats occupy garden trees in certain areas of the Republic, and some insectivorous bats roost above ceilings in many houses. However, at present there is no evidence to suggest that South African Chiroptera are possible vectors of the rabies virus and their role as vectors of rabies-related viruses seems insignificant. Since 1973, 410 bats have been examined for rabies by the Veterinary Research Institute at Onderstepoort and only 14 (30/0) have been found positive for 421 Mammals examined for rabies at the Veterinary Research Institute for the two years 1980 and 1981. Subject No. of samples Samples positive 0/0 Positive Cattle 256 87 34 Meerkat 575 186 Jtl Dog 934 199 22 Bat 368 14 4 (rabies-related virus) rabies-related virus. However. care should be taken in the interpretation of these figures. since the sample represents bats from onIya small part of South Africa. Ofthe 410 bats examined, 363 (89"10) werefrom Natal, 34 (8"10) were from the Transvaal, 8 (2070) were from the Cape Province,S (1 OJo) were from the Orange Free State. In other words, few records exist for the three largest provinces. Furthermore, Pietermaritzburg and especially Durban, where the majority of these bats were collected, fall well outside the enzootic area for rabies,) although the area from Durban northwards falls within the canine epizootic area.3 Nevertheless. no rabies virus has been identified in any of the Durban bats. Of the 14 positive cases identified, 13 (93"10) were from Durban and proved to be Lagos bat virus. Only one positive case was identified from another province. at Louis Trichardt in the Transvaal. It is still not known whether the active agent is Lagos. Duvenhage or rabies virus. With a single exception, aU bats examined from Natal were collected during the two years 1980 and 1982, with the majority(71"10) in 1980. This outbreak of rabies-related disease mainly in the fruit-eating bats of Natal coincided with an apparent upsurge of canine rabies in the province.6 This has resulted in people sending anything that moves to the Veterinary Research Institute to be tested for rabiesmfection. Furthermore, because the vast majority of these bats have not been identified, with the exception of some fruit-eating bats from Natal, we do not know whether the Lagos bat virus also occurs amongst insectivorous bat species. In most of the positive cases of Lagos bat virus, the species involved was the fruit-eating Epomophorus wahlbergi. Perhaps this virus is restricted mainly to fruit-eating bat species. Lagos bat virus was first isolated in Nigeria in 1956 from an apparently healthy fruit-eating bat, Eidolon he/vum.' Because fruit-eating bats are widely distributed in Africa, terrestrial mammals may not be involved in the spread of this virus. 6 The contribution of bats as carriers of rabies and rabies-related viruses is insignificant compared with that of other South African mammals, as is apparent from the table. Nothing is known about the role South African Chiroptera play as vectors of rabies. There is only one case of a person dying after being bitten by a bat in the Republic, apparently as a result of Duvenhage virus. In contrast. in the United States 300fthe 39 nonhaematophagous bat species8 are carriers of rabies and bats are regarded as the number one public health hazard.2 However, Greenhall' considers that the impact of bats as a public health hazard has been greatly exaggerated. In the 26 years between 1951 and 1976, only 12 documented cases of human rabies in the world were attributed to insectivorous bats.2.9 Of these, 10 were from the U.S.A. and Canada, of which only eight could be attributed to ac· tual bites of rabid bats, whereas two deaths were probably due to aerosol transmission of rabies. 2.9 However, although these cases are few, the transmission of rabies to man, to domestic animals and to wildlife by rabid non-haematophagous bats should not be underestimated. We do not know how many undocumented cases there have been, especially in developing countries. Although cases of bats showing the furious form of rabies and attacking people will Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2010). 422 be obvious and therefore well documented, those, perhaps the majority, suffering from paralytic or dump rabies as well as atypical forms will pass unnoticed. Records exist of solitary insectivorous bats attacking people. 10-13 However, most colonial bats apparently do not become violent, 14 although the only known human fatality caused by the violent behaviour ofa bat in South Africa was due to the highly colonial Miniopterus schreibersi nata/ensis. If rabid bats exist in South Africa, they may have been overlooked because bats generally are traditionally given little close attention by both scientists and the general public. Bats and man Transmission of the rabies virus will be successful only if the victim is bitten where the teeth can puncture the skin. The teeth of some of South Africa's most abundant bats are so minute that they cannot puncture the skin except when they bite somebody, for example, on the lips. One of the most common cavern dwelling bats in South Africa is the genus Miniopterus; the species M. s. natalensis is distributed throughout the Republic. ls In the Transvaal this species is both the most abundant and also the best studied. It forms clusters or colonies of a few hundred to a few thousand individuals. 16 They migrate between the southern Transvaal highveld and the northern Transvaal bushveld..17 During the autumn and winter mont.hs they form pairing and hibernating colonies on the southern Transvaal highveld, while during the spring and summer months, large maternity colonies are formed by females in caves in the nothern Transvaal bushveld. Pregnant females congregate in these maternity caves from about the beginning of October to the beginning of February; parturition takes place from the beginning of Nov.ember to the middle of December. Numbers of females at this time are estimated to be Ito 000 at Sandspruit Cave No. I and 59 000 at Peppercorns Cave. IUS In South Africa only one case is known of a human being having been bitten by a bat and who later died of rabies. 3 Unfortunately, the bat was not collected for identification, although circumstantial evidence indicates strongly that it wasM. s. natalensis. The victim, a man in his early thirties, who was taken to the H. F. Verwoerd Hospital in Pretoria on 20 February 1970, had been bitten on the lip by a bat while he was asleep about five weeks earlier. The farm Tooyskraal where the incident occurred is west of Warm baths, ncar Rooiberg, and on the main migration route of these bats between the southern Transvaal high veld and the northern Transvaal bush veld. The farm is 38 km from the Sandspruit maternity cave, and thus faUs within the hunting range of these bats. Because these bats are small (- 10 g) and have a high metabolic rate"especially while lactating and immediately afterwards when they must have enough energy for their return flight to the high veld caves, they can only occasionally avoid a night or two without feeding. Therefore, all farms within a 40 km radius of the cave may be swarmed by Miniopterus during the evenings. Around 20 January all females and young are still present at the maternity caves, as these colonies only start dispersing in February. No other bat species breed in Sandspruit Cave No. 1 and it accommodates only Miniopterus from the beginning of November onwards. Other bats present at Sandspruit Cave before November include only a few individual Hildebrandt's horseshoe bats and some hairy bats. In the prematernity cave known as Rookpoort Guano Cave, 10 km from Sandspruit Cave No. I, a few other bat species with young can be found during the period when parturition at Sancispruit Cave No.1 is in progress. These include about 100 Rhinoiophus simulator, 50 Cleiotis, 10 Myotis and 8 Nycteris with their young. The chances are, therefore, that the bat responsible for the death of the young man was M. s. nata/ensis. According to Meredith (personal communication), both the Duvenhage virus as well as the Lagos bat virus have not been idenSouth African Journa/ of Science Vol. 78 October 1982 tified in any other South African mammal. Because these bats travel great distances and cross borders and geographical barriers with ease, and come into contact with bat populations from other regions, the chances are that these rabies-related viruses are transmitted from bat to bat. [n handling thousands of bats and observing many more, I have never come across a bat reacting 'strangely'. However, a person not familiar with the behaviour of insectivorous bats, may very easily be misled into believing that a bat, especially a lone individual, is unwell. Even with the highly colonial fOnTIS such as M. s. nata(ensis, single hanging individuals are commonly found in caves. When they are approached, even during the summer months, many will make no attempt to flyaway and can even be handled for some time, when they will react very sluggishly. This is not because they are sick, but because. they are capable of reducing their body metabolism and therefore their temperature when at rest. The only time one can see that a bat may be sick is when it attacks people or animals, when it lies on the ground making no attempt to fly, or when it flies around in broad daylight. During a number of years of intensive study, I have observed none of these phenomena. Many dead bats have been found in caves, but these were mainly juveniles who became dislodged from the ceiling and whose mothers were unable to retrieve them. Dead adult bats have also been found in caves near Pretoria, but they had been killed by children or sadistic adults. The chances of a human detecting a grounded bat, especially outside the caves, are extremely small. It is much more likely that it will be spotted and t<impered with by a domestic animal such as a dog or cat or else by wild animals such as members of the Felidae, Viverridae or Canidae. As a consequence, it is possible that a disease carried by the bat may be transmitted indirectly to man. I am grateful to Dr B. J. H. Barnard, Veterinary Research Institute, Onderstepoort, for advice and for aJlowing me access to records of animals being examined for rabies. I. West G.P. (1972). Rabies in AnimalsandMan. DavidandCharles, Newton Abbot. Devon. 2. Greenhall A. M. (1982). House bat management. U. S. Filh. Wild/. Serv., Resour. Pub!. 143, Washington, D.C. J. Meredith C.D., Rassouw A.P. and van Praag Koch H. (lfJ7I). S. A/r. med. 1. 45, 767 ·-769. 4. WHO Expert Committee on Rabies (1966). Fifth Report, Wid Hlth. Org. (ech. Rep. Sen'., No. 321. Geneva. 5. Steele J.H. (1966). International aspects of veterinary medicine and ih relation to health, nutrition and human welfare. Milil. Med. IJ1, 765 -778. 6. Crick J., Tignore G.H. and Moreno K. (1982). A new isolate of Lagos bat viru~ from the Republic of South Africa. Trans. R. Soc. (rop. Med. Hyg. 76,211213. 7. Boulger L.R. and Porterfield J.S. (1958). Isolation of a virus from Nigerian fruit bats. Trans. R. Soc. (rap. Me<!. Hyg. 5Z t 421-424. B. Constantine D.G. (1979). An updated Ji~t of rabies-infectC'd bats in North America. 1. Wild. Dis. IS, 347 ~ 349. 9. BaerG.M. (1975). [n TheNaluraf HistoryojRabies, vol.ll,edit. a.Yr. Dacr, chap. 5, pp. 79-97. Academic Press, New York. 10. Kough R.H. ([954). Attack on ahuman being by a rabid insectivorous bat. 1. Am. moo. Ass. 155,441. II. Venters H.D. el al. (1954). Rabies in bats in Florida. Am. 1. pub!. Hlth 44, 182-185. 12. Wiseman J.S., Davis B.1. and Grimes J.E. (1962). Rabie~infectionin the red bat, Lasiurus borealis borealis (Muller), in T ex.:as. 1. Mammal. 43, 279 -280. JJ. Witte £.1. (1954). Bat rabies in Pennsylvania. Am. J.publ. Hlth 44, 186-188. 14. Davis R.B., Herreid II C.F. and Short H.1. (1962). Mexican free-tailed bats in Tex.:as. Em!. Monogr. 32.311346. 15. Hayman R.W. and Hill J.E. (1971). In The Mammals 0/ A/rica: an Identification manual, edit. 1. Meester and H.W. Setzer, part 2, pp. 173. Smithsonian Institution, Wa~hjngton, D.C. 16. van der Merwe M. (973). Aspects of social behavior of the Natal clinging bat Miniopterus schreibersi natalensis (A. Smith, 1834). Mammalia 37,379389. 17. Van der ~erwe M. (1975). Preliminary study on the annual movements of the Natal clinging bat. S. A/r. 1. Sci. 71,237 -241. 18. Van del Merwe M. (l978). In Proc. IVlh Int. Bat Res. Co!Jf., ewt. R.J. Olembo, 1.B. Castelino and F. A. Mutere, pp. 309322. Kenya National Academy for Advancement of Art~ and Sciences, Nairobi. Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2010).