W8: Sylvatic Rabies

Overview of Zoonotic Epidemiology: Sylvatic Rabies

Definition and Scope: Rabies is discussed in the context of sylvatic (wildlife) epidemiology, distinct from the primary global issue of canine rabies.
Contextual Importance: Sylvatic rabies is a major concern in two primary scenarios:
- Dogs transmitting rabies to wildlife species of conservation concern.
- Wildlife transmitting rabies to agricultural livestock.
Comparison to Canine Rabies:
- Canine Rabies Model: Primary host is the domestic dog; humans serve as the secondary dead-end host.
- Sylvatic Rabies Model: Primary host is a wild animal; livestock serve as the secondary dead-end host.

Sylvatic Rabies in the European Context

Historical Timeline:
- A major epidemic began in Europe following World War II.
- The origin is uncertain, though it is hypothesized to have jumped from domestic dogs to wildlife during the war.
- Spread Rate: The disease moved from East to West at a rate of $20-60\,km$ per year.
- Geographic Reach: By the 1980s, the epidemic reached mid-France.
Affected Wildlife Species (1987 Data, $N = 163,052$ total cases):
- Red fox (primary carrier in Europe).
- Raccoon dog.
- Raccoon.
- Wolf.
- Badger.
- Marten and other mustelids.
- Other carnivores.
- Wild boar.
- Roe deer, Red deer, and Fallow deer (serving as dead-end hosts).
Affected Domestic Species (1987 Data, $N = 83,270$ total cases):
- Dog and Stray dog.
- Cat.
- Cattle.
- Equine species.
- Goat/Sheep.
- Pig.
Trends in Rabies Cases (1987–2014):
- Domestic Animals: Cases dropped from $83,270$ in 1987 to $3,467$ in 2014.
- Wildlife: Cases dropped from $163,052$ in 1987 to $2,813$ in 2014.
- Bats: Cases dropped from $961$ in 1987 to $33$ in 2014.
- Humans: Cases dropped from $239$ in 1987 to $7$ in 2014.

Epidemiological Modeling of Fox Rabies

Management History: Historically, management relied on culling foxes. This failed because it required killing too many foxes too quickly and caused "perturbation effects" (changes in movement patterns) that hindered disease control.
The Compartmental Model (SEI): To understand spread and devise vaccination strategies, a three-class model is used:
- 1. Susceptible ( $S$ ): Animals capable of catching rabies.
- 2. Exposed ( $E$ ): Animals in the incubation period; infected but not yet infectious.
- 3. Infectious ( $I$ ): Rabid individuals capable of transmitting the virus.
Biological Parameters in Foxes:
- Reproduction: Population growth occurs only via the Susceptible class.
- Gestation: Approximately $53\,days$ .
- Lactation: Approximately $4-6\,weeks$ .
- Cub Dependency: Continues for several weeks after lactation; total dependency is approximately $15-20\,weeks$ .
- Incubation Period: $2-12\,weeks$ .
- Infectious Period: Less than $10\,days$ .
Model Variables and Rates:
- $S, E, I$ : Densities of Susceptible, Exposed, and Infectious individuals.
- $b$ : Per capita birth rate.
- $d$ : Per capita natural death rate.
- $r$ : Per capita mortality rate specifically due to rabies.
- $\beta$ : Transmission coefficient (rate of transmission between $S$ and $I$ ).
- $\sigma$ : Progression rate from Exposed to Infectious (incubation period inverse).
- $\gamma$ : Strength of density-dependent effects.
- $N$ : Total population density ( $N = S + E + I$ ).
- $K$ : Carrying capacity of the environment.
Mathematical Equations:
- General Growth: $\frac{dN}{dt} = rN \times (1 - \frac{N}{K})$
- Susceptible Class: $\frac{dS}{dt} = bS - dS - \beta SI - \gamma SN$
- Exposed Class: $\frac{dE}{dt} = \beta SI - dE - \sigma E - \gamma EN$
- Infectious Class: $\frac{dI}{dt} = \sigma E - dI - rI - \gamma IN$

Vaccination Strategies and Modeling Results

Vaccination Goal: The objective is to reduce the number of susceptibles until the basic reproduction number ( $R_0$ ) is less than 1 (R_0 < 1).
Model Predictions for Successful Eradication:
- Low Fox Density ( $1\,fox/km^2$ ): Requires vaccinating approximately $40-50\%$ of the population.
- Typical Rural Fox Density ( $2\,foxes/km^2$ ): Requires vaccinating approximately $60-70\%$ of the population.
- High Fox Density ( $5\,foxes/km^2$ ): Requires vaccinating approximately $90\%$ of the population.
Operational Challenges for Wildlife:
- Foxes are territorial and widely spaced.
- Direct injection is impossible; oral vaccines in food baits must be used.
- Risk of non-target species consuming baits.
Bait Delivery Logistics:
- Baits are dropped from airplanes along transects of $0.5-2.0\,km$ .
- Standard bait density is $20-25\,km^{-2}$ .
Components of Effective Oral Baits:
- Palatability: Must have attractive taste and smell detectable from several meters.
- Persistence: Must survive environmental stressors like rain, heat, snow, and frost.
- Seroconversion: Must trigger an immune response without causing disease.
- Absorption: Designed for oral absorption; if larger carnivores swallow them whole, the vaccine may not work (a drawback for multi-species targeting but a benefit for reducing non-target effects).

European Eradication Campaigns (Freuling et al., 2013)

Summary of Select Country Successes:
- Switzerland (1978–1996): Start cases: $1,054$ . Area: $38,875\,km^2$ . Cost: $6,788,657\,Euros$ .
- Germany (1983–2006): Start cases: $10,484$ . Area: $293,290\,km^2$ . Cost: $1,564,850\,Euros$ .
- France (1986–1998): Start cases: $2,465$ . Area: $147,484\,km^2$ . Cost: $1,553,178\,Euros$ .
- Estonia (2004–2009): Start cases: $314$ . Area: $41,767\,km^2$ . Cost: $142,057,754\,Euros$ .
Geopolitical Issues: While Western Europe has largely eliminated fox rabies, it remains prevalent in former "Eastern Bloc" countries due to funding and distribution difficulties. International collaboration and EU co-financing are essential to maintain a "cordon sanitaire" (buffer zone) protecting the West from resurgence.

Rabies Management and Readiness in the UK

Current Status: The UK has been rabies-free since 1922 (following muzzling laws and quarantine). Since 1922, there have been approximately 25 deaths, all involving infection acquired abroad or from local bats.
The Primary Threat: Illegal smuggling of rabid pets (dogs) that could bite an urban fox and trigger an outbreak.
Preemptive Spatial-Temporal Modeling:
- The UK uses simulations based on a hexagonal grid (better reflecting radio-tracking data than square grids).
- Models account for social structure, month-by-month mortality, and reproduction (e.g., cubs born in March, high cub mortality April–July).
- Spread Scenarios: Simulates contact rates from an index case in August, tracking spread through social groups and long-distance movements by infectious animals through October.
Bristol Field Trial: Dummy baits containing biomarkers were hand-placed in urban habitats (gardens, parks).
- Goal: $70\%$ uptake rate.
- Result: Only reached $60\%$ ; therefore, the UK does not currently seem fully prepared for an urban fox outbreak.
- Caveats: The trial assumed baits were only taken by foxes and that pets were not confined.
Scientific Uncertainties:
- Risk of dog-to-fox transfer is now considered much lower than once thought
- Behavioral Data Gap: There is almost no data on how rabid foxes behave (e.g., their range, $R_0$ in urban areas) as existing plans are built on non-rabid fox data.

Ecological Implications and Summary

Disease as Population Regulator: Data shows that as rabies cases declined due to vaccination, fox populations increased (measured by higher hunting numbers).
Human-Wildlife Conflict: Larger fox populations lead to increased conflict in farming, game shooting, and the spread of other diseases like alveolar echinococcosis.
Summary Conclusions:
- Sylvatic rabies (fox-mediated) is effectively managed in Europe through international oral vaccination campaigns.
- The modern major risk is human-mediated illegal introduction of canine rabies.
- Wildlife rabies might be secondary in importance compared to the risk of imported canine cases.