The elimination of fox rabies from Europe: determinants of success and lessons for the future

Abstract

Despite perceived challenges to controlling an infectious disease in wildlife, oral rabies vaccination (ORV) of foxes has proved a remarkably successful tool and a prime example of a sophisticated strategy to eliminate disease from wildlife reservoirs. During the past three decades, the implementation of ORV programmes in 24 countries has led to the elimination of fox-mediated rabies from vast areas of Western and Central Europe. In this study, we evaluated the efficiency of 22 European ORV programmes between 1978 and 2010. During this period an area of almost 1.9 million km² was targeted at least once with vaccine baits, with control taking between 5 and 26 years depending upon the country. We examined factors influencing effort required both to control and eliminate fox rabies as well as cost-related issues of these programmes. The proportion of land area ever affected by rabies and an index capturing the size and overlap of successive ORV campaigns were identified as factors having statistically significant effects on the number of campaigns required to both control and eliminate rabies. Repeat comprehensive campaigns that are wholly overlapping much more rapidly eliminate infection and are less costly in the long term. Disproportionally greater effort is required in the final phase of an ORV programme, with a median of 11 additional campaigns required to eliminate disease once incidence has been reduced by 90 per cent. If successive ORV campaigns span the entire affected area, rabies will be eliminated more rapidly than if campaigns are implemented in a less comprehensive manner, therefore reducing ORV expenditure in the longer term. These findings should help improve the planning and implementation of ORV programmes, and facilitate future decision-making by veterinary authorities and policy-makers.

Keywords: efforts/expenses; elimination; endgame; fox rabies; influencing factors; oral rabies vaccination.

Figure 1.

Reported annual rabies cases in Europe and extent of ORV programmes. The dashed line shows cases in countries which eliminated rabies (see table 1) and the solid line shows the total number of cases for all countries in Europe. Cases in bats and humans are excluded. The maximum area covered by oral rabies vaccination is shown in km².

Figure 2.

ORV effort and rabies cases. (a) Spatial extent of ORV area and the total number of ORV campaigns conducted in each country between 1978 and 2010. Reported rabies cases in (b) 1983 and (c) 2010.

Figure 3.

Factors influencing the efficiency of ORV programmes in the control and elimination of rabies. To illustrate the influence of the area index (I) and of the proportion of the territory ever affected (P) on numbers of campaigns to (c,d) control and (a,b) eliminate rabies, the continuous variables I and P are set to low and high values within the range of observed values. In (a,c) I is set to 0.2 (solid line) and 1.0 (dashed line) while P is set to 0.95 (median). In (b,d) P is set to 0.02 (dashed line) and 1.0 (solid line) while I is set to 0.65 (median). All curves are generated using parameter estimates obtained from the statistical analysis together with values for the influential parameter as described above. Survival curves are plotted as cumulative events, f(y) = 1 − y, and hash marks denote censored points.

Figure 4.

Estimated effort required to reduce rabies incidence. Accumulated financial expenditure (in euro) versus the proportional reduction in rabies cases from initial endemic levels. The inset shows the linear regression of log_e transformed annual rabies incidence (y-axis) against cumulative costs (x-axis) in million euros. A mixed model with country as a random effect was used to estimate λ (in equation (2.3). The fixed effect coefficient λ (−0.926) was used in the modelled relationship of the exponential decline in rabies incidence with increasing cumulative expenditure on ORV according to equation (2.3).