During the study period, animals from the Aegean region suspected of having rabies were submitted for rabies diagnosis to the Bornova Veterinary Control and Research Institute in Izmir. Routine rabies diagnosis was based on detection of Negri bodies, followed by fluorescent antibody test results; for negative samples, the mouse inoculation test was also performed (3). From 1998 through 2007, a total of 3,737 specimens were submitted; of these, 118 samples could not be examined because the samples were of poor quality (Table 1). Analysis of the data for the 3 major animal species submitted (cattle, dogs, and foxes) during this period showed dramatic changes in the number of rabies cases for each of these species (Table 2). In 1998, no rabies in foxes was reported, and dogs clearly dominated rabies submissions. However, in subsequent years, rabies emerged in foxes; this emergence coincided with an increased number of rabid cattle reported and a decreased number of rabid dogs. The annual number of rabid dogs correlated only weakly with total number of dogs submitted for testing; coefficient of determination (R²) was 0.56. However, this correlation was markedly higher for cattle and foxes (R² = 0.99 for both species). This finding indicates that the lower number of rabid dogs did not result only from decreased surveillance for this species.

Figure 2

Figure 2. Location of rabies cases in the 3 most affected species in Aegean region by year, 1998–2007. Red, red foxes; green, dogs; blue, cattle.

From 1998 through 2000, almost all cases in the 3 most affected species were reported from the area between the cities of Izmir and Manisa (Figure 2), and the epizootic progressed in a wave-like fashion southward; in 3 years, the area of rabies cases moved ≈150 km. In 2003, the southeastward movement of the rabies epidemic slowed and, in 2004, appeared to halt. In 2005, cases again increased in the northern part of Aydin Province, which borders Izmir Province. In 2006, no clear movement of this outbreak was observed.

The northern Aegean region may not be a suitable habitat for foxes and therefore may not have supported a sufficient number of foxes for an epizootic. Reliable data on fox density or even the number of foxes shot are lacking. Several cases of rabies in foxes were reported in 2006 from the area where the fox outbreak had started 7 years earlier. In 2007, rabies in foxes was still reported from this area, and the outbreak in Aydin had moved eastward and established itself in the neighboring province of Denizli.

The high number of free-roaming dogs and the low vaccination coverage of the dog population would have provided ample opportunities for infected dogs to transmit the virus to foxes. Hence, foxes (or a fox) in the Izmir area are assumed to have become infected, and rabies then spread in the fox population. The close association of the sequences of rabies virus isolates from dogs and foxes in this area supports a recent transfer (2). However, the phylogenetic data provide no indication of the direction of virus transmission. The lack of reported rabies in a fox in this area since 1986 suggests that dogs transferred the virus to foxes, leading to the present rabies outbreak, not the reverse.

Since 1999, rabies has moved predominantly south and southeast at ≈40–50 km per year from the area where the first cases in foxes were reported. This movement was associated with increases in the number of rabies cases in foxes and cattle until 2003, when the number of cases sharply declined after mass vaccination of cattle. Since 2003, the numbers of rabid dogs and rabid foxes reported each year has remained approximately the same. However, the number of dogs submitted for rabies diagnosis is ≈9× higher than the number of foxes submitted. Furthermore, only 20% of the dogs tested were rabies virus–positive, compared with almost all (95%) of the foxes; therefore, the true number of rabid foxes can be assumed to exceed the number of rabid dogs.

Although during the 10 years of the study period, 6 cases in humans in the study area were reported, none were linked to foxes. Hence, the public health risks associated with rabid foxes are relatively small compared with those associated with rabid dogs. However, if not eliminated, rabies in foxes will form a reservoir for disease persistence. A high number of rabies cases in cattle causes an economic loss. Mass vaccination of cattle reduces these losses but does not solve the problem. After the initial epizootic, the disease seems to have become endemic to the Aegean region. Preventing the spread of rabies to foxes in unaffected areas is crucial. Therefore, to control the present outbreak, a campaign to orally vaccinate foxes against rabies in the affected provinces of Turkey was initiated during February 2008 and conducted again in 2009.