Designing programs for eliminating canine rabies from islands: Bali, Indonesia as a case study

<p>Background: Canine rabies is one of the most important and feared zoonotic diseases in the world. In some regions rabies elimination is being successfully coordinated, whereas in others rabies is endemic and continues to spread to uninfected areas. As epidemics emerge, both accepted and contentious control methods are used, as questions remain over the most effective strategy to eliminate rabies. The Indonesian island of Bali was rabies-free until 2008 when an epidemic in domestic dogs began, resulting in the deaths of over 100 people. Here we analyze data from the epidemic and compare the effectiveness of control methods at eliminating rabies.</p> <p>Methodology/Principal Findings: Using data from Bali, we estimated the basic reproductive number, R0, of rabies in dogs, to be ~1·2, almost identical to that obtained in ten–fold less dense dog populations and suggesting rabies will not be effectively controlled by reducing dog density. We then developed a model to compare options for mass dog vaccination. Comprehensive high coverage was the single most important factor for achieving elimination, with omission of even small areas (<0.5% of the dog population) jeopardizing success. Parameterizing the model with data from the 2010 and 2011 vaccination campaigns, we show that a comprehensive high coverage campaign in 2012 would likely result in elimination, saving ~550 human lives and ~$15 million in prophylaxis costs over the next ten years.</p> <p>Conclusions/Significance: The elimination of rabies from Bali will not be achieved through achievable reductions in dog density. To ensure elimination, concerted high coverage, repeated, mass dog vaccination campaigns are necessary and the cooperation of all regions of the island is critical. Momentum is building towards development of a strategy for the global elimination of canine rabies, and this study offers valuable new insights about the dynamics and control of this disease, with immediate practical relevance.</p&gt

Lessons for rabies control and elimination programmes: a decade of One Health experience from Bali, Indonesia

This Review discusses the advancements made and challenges remaining in One Health around endemic and emerging zoonotic diseases, food safety and food security, antimicrobial resistance, wildlife diseases, and other issues that impact health such as poverty. It highlights the added value of using a One Health approach to coordinate, collaborate, and communicate across multiple sectors and disciplines to address complex health threats at the human-animal-environment interface with the goal of improving health for all. This issue also provides innovative ideas to apply a One Health approach toward the following areas: strengthening human and animal health systems, One Health mechanisms and activities to enhance subnational, national, regional, and global health, synergising tools for capacity assessment and One Health operationalisation across sectors, better integrating wildlife and environmental health, disaster response, reduction of poverty, prevention and control of zoonoses, and progress toward rabies elimination. Collaboration using One Health principles could greatly increase trusted networks for coordination across sectors, help improve global health outcomes, and reduce health threats. Barriers to One Health can be significant and typically include institutional capabilities and culture, poor communication and information sharing across sectors, limited personnel resources, and budgetary constraints. Fortunately, the need for multisectoral, One Health collaboration at the local, national, regional, and global levels is being recognized and steps are being taken to implement and operationalise One Health. Multiple success stories of One Health in action exist and provide real-world examples of the benefits of using a multisectoral, One Health approach. This review aims to shine a light on successes, remaining challenges, and implementation of a multisectoral, One Health approach to decrease the global disease burden in people and animals while promoting environmental health

Model description.

<p>(A) Secondary cases are drawn from the (i) offspring distribution, and become infectious at a date drawn from the (ii) generation interval distribution: here four secondary cases are generated by the index case (black dot) which become infectious on day 14, 21, 23, and 35. The occurrence of secondary cases depends on vaccination coverage in the grid cell at the time of transmission. (iii) With probability 1–<i>p</i> each offspring occurs at a location generated from the local dispersal kernel (solid black arrows). (iv) With probability <i>p</i>, each offspring occurs on any randomly chosen grid cell (broken black arrow). It took 2.2 years for rabies to be detected in all nine Regencies (grey band), consistent with <i>p</i> = 0.05–0.09 (black dots are medians with 95% PIs from 100 simulations). See <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t001" target="_blank">Table 1</a> for parameterization of distributions. (v) Human rabies deaths versus confirmed dog rabies cases, showing the best-fit relationship (black line, see <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#s3" target="_blank">Results</a> for equation) and 95% confidence intervals (grey area). (B) 95% PI envelope of simulated cases (grey area) with annual campaigns of the ‘random’ mass vaccination strategy (green line, <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t002" target="_blank">Table 2</a>), which is rolled out when cumulative cases reach 7,000 and from which point the time to eradication is measured.</p

Vaccination strategies.

<p>The probability of eradication following: (Ai) 1; (Aii) 2; (Aiii) 3 campaigns under a range of coverages (40, 60, 80%) and inter–campaign intervals (0, 6, 12 months); (Aiv) vaccination as implemented on Bali, and projected from January 2012 when rabies was still circulating. The time to eradication (medians with 95% PI) for a range of: (B) frequencies of human–mediated transport of dogs (<i>p</i> = 0, 0.02 or 0.05) and campaign strategies (<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t002" target="_blank">Table 2</a>). 95% PI of the one-month ‘sync’ strategy is highlighted (grey band) for comparison with the six–month strategies; (C) coverages when campaigns last 1 month or 6 months. (D) The probability of eradication with % island area left unvaccinated, made up of either randomly chosen 1 km squares (solid lines) or randomly chosen blocks, and when human-mediated movement of dogs was either infrequent (<i>p</i> = 0.02, grey) or frequent (<i>p</i> = 0.05, black).</p

Key epidemiological and operational variables determining the success of rabies vaccination programmes in terms of the predicted probability of eradication (grey y–axis and line) and time to eradication (black y–axis, medians and 95% PI), showing sensitivity to: (A) the basic reproductive number, <i>R</i>₀, (B) vaccination coverage (achieved at the time and location of the campaign (see Fig. 4)), (C) annual dog population turnover, with conversion into birth/death rate assuming constant population size (birth rates equal to death rates), and (D) duration of immunity provided by vaccine.

<p>Based on 1000 simulations generated using parameters in <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t001" target="_blank">Table 1</a> (unless specified) and annual campaigns of the ‘random’ mass vaccination strategy (<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t002" target="_blank">Table 2</a>).</p

Parameters values and distributions used to model rabid dog movement and transmission processes.

<p>Parameters values and distributions used to model rabid dog movement and transmission processes.</p

Trajectories of vaccination coverage achieved at the island-wide level during modeled vaccination campaigns and in relation to levels of coverage required for herd immunity.

<p>Three types of coverage are referred to in the text: target coverage achieved in the subset of the population at the time and location of a local campaign (i.e. within a block); island-wide vaccination coverage (y-axis); and critical vaccination coverage (<i>P_crit</i>) which is required for herd immunity and is determined by <i>R</i>₀, the basic reproductive number of rabies in Bali, <i>P_crit</i> = 1-(1/<i>R</i>₀). <i>R</i>₀ estimated for Bali is 1·2, which corresponds to a <i>P_crit</i> of 17% (grey solid line). A 40% coverage campaign resulted in a trajectory that stayed above 17% (black solid line) and the probability of eradication was 1 (<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-g003" target="_blank">Fig. 3B</a>), whereas 30% coverage resulted in a trajectory that dipped below 17% (black dashed line) and the probability of eradication was less than 1 (<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-g003" target="_blank">Fig. 3B</a>). Annual campaigns were modeled, using parameters in <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t001" target="_blank">Table 1</a> and the ‘random’ six-month strategy (<a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-t002" target="_blank">Table 2</a>). Blocks are assumed to be vaccinated at the end of the month hence coverage increments jaggedly. Coverage declines between vaccinations due to waning of immunity and dog population turnover.</p

Modelled vaccination strategies.

<p> All campaigns were annual unless specified in the analyses.</p

Rabies incidence and spread in Bali prior to island-wide mass vaccination.

<p>(A) Cases in humans and dogs and corresponding control efforts. (B) The month that rabies was first confirmed in each village. The black dot marks the village where the index case occurred. Regencies are outlined in black.</p

The vaccination campaigns on Bali and prospects for rabies eradication.

<p>Observed confirmed dog cases up to December 2011 (solid red line) overlay model confirmed cases (grey area, shaded according to confidence level) simulated from estimated vaccination coverage in the Bali dog population (solid blue line) and assuming 0.07 probability of confirming a case <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd.0002372-Townsend1" target="_blank">[6]</a>. For 3 scenarios, vaccination coverage was projected forward to December 2014 (broken blue lines), and implemented in the model to project upper percentile limits for confirmed cases (broken red lines) and the probability of island-wide eradication (see legend and <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0002372#pntd-0002372-g003" target="_blank">Fig. 3Aiv</a>). The increase in cases in Dec 2011 may have been due to a substantial improvement in surveillance involving follow up of suspected animal bite cases by outbreak investigation teams.</p