Indirect oral immunization of captive vampires, Desmodus rotundus
Introduction
The use of preventive vaccines against rabies largely contributed to the reduction or local eradication of rabies in domestic animals. Therefore, it would be natural the attempt to vaccinate wild animals. However, the control of rabies in wildlife population, which replaced dogs as reservoirs and vectors of rabies, required other strategies such as the successful oral vaccination of wild mammals in Europe.
Since 1978, several European countries conducted oral rabies vaccination programs for terrestrial wildlife. One of the vaccines used in the field is V-RG, a recombinant vaccinia virus, which expresses the glycoprotein of rabies virus (Kieny et al., 1984). Millions of baits containing V-RG vaccine were distributed in the last decade in Canada, United States, Switzerland, Germany, Belgium and France. Programs of oral vaccination of red foxes (Vulpes vulpes), raccoons (Procyon lotor) and coyotes (Canis latrans) were successful in eliminating rabies from large areas (Brochier et al., 1991, Pastoret et al., 1988, Hanlon et al., 1998, MacInnes et al., 2001).
In countries where progress has been made in terms of human rabies prevention, bats have been responsible by a significant proportion of human infections. In the USA, from 1990 to 2000, 30 of the 32 human rabies cases were associated with insectivorous bat rabies virus variants (CDC, 2000).
In Latin America, the hematophagous bat (Desmodus rotundus) is one of the main reservoirs of rabies virus and causing heavy economic losses in livestock annually. Currently, the control of rabies transmitted by Desmodus rotundus is performed by bat population reduction using anticoagulants applied on the backs of targeted vector bats (Linhart et al., 1972). Due to their habit of hygiene, the anticoagulant agent is spread among the colony, killing between 10 and 20 bats per vector bat (Greenhall, 1965). The use of anticoagulants is still very controversial. Some investigators have proved them to be successful (Arellano-Sota, 1988) while for others the anticoagulants have been shown to produce moderate success. Yet, anticoagulants are not an effective method to stop the spread of disease (Jackson, 2002). Another control strategy, although much more expensive, is vaccination of cattle.
Analysis of animal rabies in Brazilian samples by monoclonal antibodies and molecular sequencing showed that dogs and vampire bats are the main vector reservoirs (Ito et al., 2001, Favoreto et al., 2002). The virus variant 3, characteristic of vampire bats, was isolated from 100% of cattle, horses and vampire bat samples (111) taken and in 58.3% of samples (35) of non-vampire bats, showing the importance of Desmodus rotundus as a reservoir of rabies in Brazil.
In Brazil, the number of human rabies cases has been 20–30 per year since 1994. Bats are the second most frequently identified vector-related to human rabies cases. Bat bites on humans have been reported in Brazil always associate to enviromental modifications in bats habitats (Batista da Costa et al., 1993, Scheneider et al., 2001). Recently, in two Brazilian villages of the North country, 21 people bitten by a vampire bat died of rabies. The antigenic analysis of samples from this outbreak identified the variant 3 virus. As for animal rabies in the period between 1994 and 2003, 20,590 cases of rabies in cattle, 2314 in horses and 676 in hematophagous bats and non-hematophagous bats were reported (Health Ministry from Brazil, 2004).
The objective of this study is to assess the immunogenicity of a recombinant rabies vaccine (V-RG) applied in a neutral vehicle spread on the back of hematogphagous vector bats (Desmodus rotundus), kept in captivity. Our hypothesis is that the behavior of the vampire bat (self-hygiene and intense corporal contact to each other in the colony) allows the paste mixed with an oral vaccine applied on the back of one bat to indirectly protect other bats from the same colony. This strategy may represent an alternative control method to the anticoagulant, vampiricide paste, which is decimating the population of Desmodus rotundus.
To test this we carried out a set of experiments in which we applied an oral vaccine mixed with neutral Vaseline paste on the back of one bat that was then allowed to live with 6–9 other non-pasted bats in groups distributed into special cages designed to this end. All the bats of all groups were then challenged with intramuscular injections of live rabies virus and the proportion of survivals was annotated.
Section snippets
Captivity
The bats (Desmodus rotundus) used in this experiment were adults (males and females), maintained in cages designed specially for rabies experimental purposes, at the School of Medicine of University of São Paulo. They were collected in caves of Salto do Pirapora and Salto de Itu Cities (State of São Paulo), Southeastern Brazil.
The air circulation in the interior of the cages occurred through an inlet and an outlet system with biosafety filters. The system was designed with consideration for the
Results
In the oral vaccination experiment, the proportion of bats that survived after challenge with 105 MICLD50, was 14% (Group A), 25% (Group B), 42% (Group C), 66% (Group D), and 100% (Group E). The incubation period ranged from 5 to 19 days (average 6.9 days) and the morbidity period was usually from 24 to 48 h (Table 1).
In the indirect vaccination experiment, the proportion of survivors was 42.8% (Group A), 71.4% (Group B), 57.1% (Group C), 57.1% (Group D), 71.4% (Group E), 62.5% (Group F), 55.5%
Discussion
We expected, as in the case of bat control by vampiricide paste, that the administration of V-RG vaccine through paste in one or two bats could induce immunity and so indirectly protect other bats from the same group. We think that our results are encouraging because a significant number of bats that did not receive the vaccine were indirectly immunized by contact and survived the virus challenge.
When administered directly into the mouth, the V-RG vaccine was immunogenic to hematophagous bats,
Acknowledgements
The following people provided volunteer field assistance to locating and capturing bats: Carlos Alberto Venésio Gomes from Vigilância Sanitária of Paraisópolis-Minas Gerais; Luis Carlos Ismerin and José Carlos Pinto from Escritório de Defesa Agropecuária of Sorocaba, São Paulo. We also thank Akio Sato, Cristiano Von Simson and Emílio Salani from Merial Saúde Animal Ltda. The following people provided administrative assistance: Vilma A Duarte Sanches, Valtair Santana and Ruberval da Silva from
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