Potential Eradication of Rabies from in

Scott-Orr, H (1), Bingham, J (2), Saunders, G (1), Dibia, IN (3), Putra, AAG (3) Geong, M (4). (1) NSW Department of Primary Industries, Orange, NSW, Australia (2) Australian Animal health Laboratory, CSIRO, Geelong, Victoria, Australia (3) Disease Investigation Centre, Denpasar, , Indonesia (4) Provincial Livestock Services, Kupang, Nusa Tenggara Timur, Indonesia

Abstract: Development of a potential strategy for the eradication of canine rabies from Flores is described. Rabies entered the Indonesian island of Flores in 1997 and gradually spread east to the adjacent island of Lembata and west throughout Flores island over the next seven years. It is now endemic with approximately 1000 post-exposure prophylactic treatments and some human deaths each year. Reasons for persistence of the disease despite eradication attempts include; the difficult terrain of Flores and Lembata; cultural and economic roles of dogs in Flores leading to poor cooperation with elimination attempts; the very high dog population when rabies entered; rapid turnover of the dog population and its ability to rebound quickly after population reduction programs; difficulty in catching and presenting dogs for parenteral vaccination; and low duration of immunity provided by the local injectable vaccine. However, eradication is still highly desirable to prevent further spread of rabies to other islands, as well as eliminating ongoing costs and human misery from the disease on Flores. A strategy of mass dog vaccination with effective oral and injectable vaccines is being developed to suit local conditions. Preliminary research will include studies on; dog population dynamics and their interactions with cultural and trading practices on Flores and Lembata; immunogenicity and safety of selected vaccine(s) in local dogs; epidemiology of rabies in dogs and people on Flores and Lembata; canine bait uptake and potential vaccination coverage under local conditions; and a detailed prospective cost-benefit study to justify funding of the selected strategy.

Keywords: Rabies eradication, oral vaccination, dog population dynamics and control, Indonesia, Flores.

Introduction: Flores island is located in Indonesia’s Eastern Islands archipelago at 8ºS and 121ºE, and is 17,033 km2 in area, 350 km long and up to 60km wide. The terrain is very difficult to traverse by road, with multiple active volcanoes and sharply winding roads subject to wash away and landslides, especially during the heavy tropical rainy season. Due to this there are a number of distinct language groups and local cultures on the island, and coordinated action across all districts is difficult.

The Eastern Islands were historically free of rabies, but it entered the eastern tip of Flores in 1997 at the town of , via dogs brought on a fishing boat from the island of Buton, . An attempt was made to stamp it out by dog elimination in and around the town, but this proved both unpopular and counterproductive, leading to smuggling of dogs into previously uninfected areas. Further attempts were then made to apply both vaccination and dog population control but rabies gradually spread east to the adjacent island of Lembata and west throughout Flores island over the next seven years (Table. 1). It is now endemic with over 1000 post-exposure prophylactic treatments and some human deaths each year.

Table 1 Distribution of reported human cases of dog bites and deaths due to rabies District Human 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 (east to Cases west) Lembata Bites 44 0 9 7 0 25 275 147 240 Deaths 0 0 0 0 0 0 1 0 0 Flores Bites 6 541 125 53 140 156 95 247 86 203 242 Timur Deaths 0 10 11 3 2 0 0 3 0 1 0 Sikka Bites 140 274 151 60 87 255 119 422 497 994 Deaths 0 14 2 1 0 0 0 0 3 0 Ende Bites 54 128 266 72 188 189 465 145 679 Deaths 0 4 2 1 0 0 1 0 0 Ngada Bites 1780 62 62 202 318 382 168 371 Deaths 50 4 0 4 3 5 2 1 Manggar Bites 326 650 802 652 348 1,298 544 423 ai Deaths 2 2 7 2 1 9 1 4 Manggar Bites 52 173 104 143 ai Barat Deaths 0 5 0 0 Total Bites 6 681 497 2,438 1,187 1,186 1,392 1,298 3,101 1,808 3,092 Deaths 0 10 25 61 8 8 6 7 21 7 5

Methods: As part of an ACIAR project (“Improving veterinary service delivery in a decentralised Indonesia”), a study has been made of the reasons for spread and persistence of rabies on Flores despite attempts to stop it by ongoing control measures of vaccination and elimination of dogs. Workshops were held in Flores in May 2008 and May 2009 with input from the Indonesian central, provincial and all relevant district health and veterinary government services, as well as Indonesian and Australian specialists. In May 2008 the Australian project team members made a journey throughout the length of Flores with visits to local governments and typical rural, urban and peri-urban villages, to understand local attitudes and practices which might influence rabies eradication attempts. Five postgraduate students have also been selected and funded by the ACIAR project to study various aspects of rabies epidemiology, the Flores dog population and the possibility of using oral rabies vaccine as part of an eradication strategy. Options for improved control and eradication strategies will be developed using information from this research and a preferred strategy selected after cost benefit analysis of the options.

Results: Apart from the difficult terrain and geography of Flores and Lembata, there are many contributing factors to the failure of rabies eradication to date. Dogs have high cultural and economic value in Flores. They are eaten as a major source of animal protein and are required for particular ceremonies in different parts of the island. This leads to a lot of dog trading between districts and the import of dogs from other islands due to high price differentials especially at key times like Christmas. They are also highly valued as guards, both around the house and village but also to guard crops on steep mountain sides from wild pigs and monkeys. As well, they are used for hunting wild deer and pigs, and are considered essential companions for fishermen undertaking long boat trips in small boats. When rabies entered Flores, there was a very high dog population (Table 2) and despite repeated and continued population reduction programs, the dog population rebounded quickly. Rapid population turnover confounds attempts to achieve satisfactory levels of vaccination coverage of the dog population. Local veterinarians report that up to 90% of dogs presented for vaccination each year have not previously been vaccinated. As most dogs are free ranging and unrestrained, it is difficult to catch and present them for parenteral vaccination. As well as this, the locally produced killed rabies vaccine has a relatively low duration of immunity and a booster vaccination is recommended at three months, but rarely implemented.

Table 2: Changes in dog and human population density on Flores and Lembata over time 1997 2003 2005 2007 Dog Population 636,015 169,035 250,372 203,478 Dogs per Km2 37 10 15 12 Human Population 1,566,127 1,547,226 1,757,952 1,777,472 No. of Families 313,225 309,445 351,590 355,494 Dog per person 0.4 0.1 0.14 0.11 Dogs per family 2.03 0.55 0.71 0.57

When rabies entered Flores in 1997, the population of dogs was estimated at over 600,000 head, with a mean density of 37 dogs per km2 (Table 2). This density is very high and highly conducive to the transmission and maintenance of rabies. The density of susceptible dogs must be reduced to below five dogs per km2 to have reasonable prospects of preventing rabies from cycling in the population. This may be done by either eliminating dogs or by vaccinating them with an effective vaccine.

In Indonesia the policy for dealing with a rabies incursion into a previously uninfected island is to cull dogs first, then, if that fails, to apply vaccination and selective elimination. This broadly follows World Health Organisation guidelines. Implementation of this policy on Flores sequentially in each new district infected was unproductive. There was considerable community resistance, some dogs were concealed from the local authorities, and some were smuggled to areas where control was not yet occurring. This hastened rabies spread and frustrated local control efforts. Some districts brought in regulations allowing only two dogs per household, so that only two dogs are presented by each family for registration and vaccination, while others may be hidden from the vaccinating teams or taken away to the forest while the team is in the area. Therefore dog population numbers reported since 1998 are likely to be significantly lower than the actual population, even though in many districts a rise in reported dog numbers was evident after a sharp initial decline.

Vaccination of animals susceptible to rabies (dogs, cats and pet monkeys) was first implemented in 2001 and has been applied ever since, along with continued “partial elimination” of dogs, with variable intensity and success. An international vaccine with a three year duration of immunity was first used, and then a cheaper locally produced vaccine, which requires a booster dose at 3 months to give a 12 month duration of immunity. The target has been for 80% vaccination coverage of the susceptible population and 20% elimination, but on average the achievement against targets has been between 30-80% vaccination and 10% elimination of the recorded population (which is likely to be a significant underestimate in some districts as noted above).

Discussion: A strategy of mass dog vaccination with effective injectable and oral vaccines is being developed to suit local conditions on Flores. This strategy would involve coordinated delivery to the field in Flores and Lembata’s nine districts of refrigerated oral vaccine, either in preformulated baits or as sachets for local vaccine assembly in baits at sub-district or village level, and supervised oral vaccine administration by hand to dogs, to supplement a program of parenteral vaccination with an effective rabies vaccine. This mass vaccination would aim to achieve at least 80% coverage of the dog population across Flores and Lembata within a period of one month. It would be repeated either annually or biannually for one or more years depending on disease and population modelling as well as the results of intensive surveillance of subsequent rabies incidence in humans and dogs, and of vaccination coverage and immune response in the dog population. Precursor elements would include a comprehensive public awareness campaign for at least six months, as well as operational training and provision of necessary cold chain, transport and consumables at district, sub-district and village level.

Preliminary research to underpin development of detailed options for this strategy includes studies on dog population dynamics and their interactions with cultural and trading practices on Flores and Lembata, on the immunogenicity and safety of the selected vaccine in local dogs, on the epidemiology of rabies in dogs and people on Flores and Lembata to identify any risk factors which would affect disease eradication, and on canine oral bait uptake and potential population vaccination coverage under local conditions. As results from this research become available over the next two years, they will be used to develop strategic eradication options, as well as to establish a robust and effective surveillance program for rabies on Flores, which will underpin policy and meet monitoring requirements for rabies control. A detailed prospective cost-benefit study will be prepared to justify funding of the agreed strategy, which could serve as a model for rabies eradication elsewhere.

Conclusion: Rabies will not be eradicated from Flores and Lembata in the foreseeable future using the current tools of injectable killed vaccines and dog elimination, due to the geographic, logistical and cultural constraints outlined above. The opportunity to use an oral vaccination campaign for dogs to reach a far greater proportion of the canine population and rapidly break the rabies transmission cycle is being explored by this project. Data generated by the project’s postgraduate students will provide answers to many of the technical questions posed by this approach. There are considerable inefficiencies and costs in the current partially disconnected, stop/start approach being adopted by different kabupaten on Flores. These need to be documented in retrospective and prospective benefit cost studies and short term opportunities sought to improve coordination.

While ever rabies remains in Flores and Lembata, there is a high risk that infected dogs will be carried by fishing craft or ferries to neighbouring islands like , Sumba, Sumbawa, as may have already happened in Bali. The experience of rabies spread in Flores could easily be replicated in these islands, with huge costs in financial and human terms and an adverse effect on Indonesian tourism. There is also the possibility of further extension either via Papua or directly to northern Australia by traditional or illegal movements or fishing. Were rabies to enter northern Australia, the high numbers of poorly controlled dogs in remote aboriginal communities would pose a very difficult vector population to control and a severe diminution of quality of life in the Top End of Australia would occur.

References: WHO (2007) Oral vaccination of dogs against rabies

Acknowledgments: Support and funding for this investigation is being provided by the Indonesian Ministry of Agriculture’s Directorate General of Livestock Services and relevant provincial and district governments for Flores and Lembata, and the Australian Centre for International Agricultural Research (ACIAR).