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Abstract

Usutu virus (USUV), a flavivirus of the Japanese encephalitis virus complex, was for the first time detected outside Africa in the region around Vienna (Austria) in 2001 by Weissenböck et al. (2002). USUV is an arthropod-borne virus (arbovirus) circulating between arthropod vectors (mainly mosquitoes of the Culex pipiens complex) and avian amplification hosts. Infections of mammalian hosts or humans, as observed for the related West Nile virus (WNV), are rare. However, USUV infection leads to a high mortality in birds, especially blackbirds (Turdus merula), and has similar dynamics with the WNV in North America, which, amongst others, caused mortality in American robins (Turdus migratorius). We hypothesized that the transmission of USUV is determined by an interaction of developing proportion of the avian hosts immune and climatic factors affecting the mosquito population. This mechanism is implemented into the present model that simulates the seasonal cycles of mosquito and bird populations as well as USUV cross-infections. Observed monthly climate data are specified for the temperature-dependent development rates of the mosquitoes as well as the temperature-dependent extrinsic-incubation period. Our model reproduced the observed number of dead birds in Austria between 2001 and 2005, including the peaks in the relevant years. The high number of USUV cases in 2003 seems to be a response to the early beginning of the extraordinary hot summer in that year. The predictions indicate that > 70% of the bird population acquired immunity, but also that the percentage would drop rapidly within only a couple of years. We estimated annually averaged basic reproduction numbers between R₀=0.54 (2004) and 1.35 (2003). Finally, extrapolation from our model suggests that only 0.2% of the blackbirds killed by USUV were detected by the Austrian USUV monitoring program (Chvala et. al., 2007). These results suggest that the model presented is able to quantitatively describe the process of USUV dynamics. To investigate future scenarios, we entered temperature predictions from five global climate models into the USUV model and also considered four different climate-warming scenarios defined by the I ntergovernmental Panel on Climate Change, IPCC (20 different model-scenario combinations). We downscaled the 20 time series of predicted temperatures (through the year 2100) to represent the region around Vienna. Our simulations predict that USUV will persist in the host population after the epidemic peak observed in 2003. USUV-specific annual blackbird-mortality time series predict that the outbreak frequency increases successively from the beginning to the end of the century. Simulations of worst-case scenarios result in an endemic equilibrium with a decline of the blackbird population of about 24%. Additionally we calculated the annually averaged basic reproduction number for the period 1901-2100. The latter depict that undetected major outbreaks before 2000 were unlikely, whereas it is likely that the USUV becomes endemic after 2040.

Mean annual basic reproduction numbers for the IPCC worst-case scenarios A1 (upper panel) and best-case scenarios B1 (lower panel).

R code

USUVmodel.R

The model was developed using the R statistical computing environment (R Development Core Team, 2010).

References

Rubel, F., K. Brugger, M. Hantel, S. Chvala, T. Bakonyi, H. Weissenböck, and N. Nowotny, 2008:
Explaining Usutu virus dynamics in Austria: Model development and calibration.
Prev. Vet. Med., 85, 166-186.

Reiczigel, J., K. Brugger, F. Rubel, N. Solymosi, and Z. Lang, 2010:
Bayesian analysis of a dynamical model for the spread of the Usutu virus.
Stoch. Environ. Res. Risk Assess., 25, 455-462.

Walter, M., K. Brugger, and F. Rubel, 2018:
Usutu virus induced mass mortalities of songbirds in Central Europe: Are habitat models suitable to predict dead birds in unsampled regions?
Prev. Vet. Med., 159 , 162-170.

Acknowledgments

Parts of this work were funded by the Hochschuljubiläumsstiftung der Stadt Wien (H-1122/2006). Contributions from Katharina Brugger were supported by the research grant F130-N of the University of Vienna.