BackgroundAs a result of globalization and climate change, Dirofilaria immitis and Dirofilaria repens, the causative agents of dirofilariosis in Europe, continue to spread from endemic areas in the Mediterranean to northern and northeastern regions of Europe where autochthonous cases of dirofilarial infections have increasingly been observed in dogs and humans. Whilst D. repens was recently reported from mosquitoes in putatively non-endemic areas, D. immitis has never been demonstrated in mosquitoes from Europe outside the Mediterranean.MethodsFrom 2011 to 2013, mosquitoes collected within the framework of a German national mosquito monitoring programme were screened for filarial nematodes using a newly designed filarioid-specific real-time PCR assay. Positive samples were further processed by conventional PCR amplification of the cytochrome c oxidase subunit I (COI) gene, amplicons were sequenced and sequences blasted against GenBank.ResultsApproximately 17,000 female mosquitoes were subjected to filarial screening. Out of 955 pools examined, nine tested positive for filariae. Two of the COI sequences indicated D. immitis, one D. repens and four Setaria tundra. Two sequences could not be assigned to a known species due to a lack of similar GenBank entries. Whilst D. immitis and the unknown parasites were detected in Culex pipiens/torrentium, D. repens was found in a single Anopheles daciae and all S. tundra were demonstrated in Aedes vexans. All positive mosquitoes were collected between mid-June and early September.ConclusionThe finding of dirofilariae in German mosquitoes implies the possibility of a local natural transmission cycle. While the routes of introduction to Germany and the origin of the filariae cannot be determined retrospectively, potential culicid vectors and reservoir hosts must prospectively be identified and awareness among physicians, veterinarians and public health personnel be created. The health impact of S. tundra on the indigenous cervid fauna needs further investigation.
After the repeated demonstration of Dirofilaria repens infections in German dogs, D. repens and Dirofilaria immitis DNA was detected in mosquitoes trapped in 2011, 2012 and 2013 in northeastern and southwestern Germany within the framework of culicid monitoring projects. As temperature is the most important factor dictating the extrinsic development of dirofilarial larvae in the potential vector, data of the German Weather Service (DWD) were analysed for the regions where the positive mosquitoes had been collected. Based on the mean daily temperatures recorded by weather stations most closely to the collection sites of the mosquitoes, it can be concluded that the mosquitoes were trapped in time periods that allowed for the completion of the developmental cycle of the worms in the mosquitoes and a subsequent transmission to a vertebrate host. The results of this study confirm the principal climatic suitability of certain German regions for the establishment of natural dirofilarial transmission cycles. Moreover, the theoretical climatic considerations, together with findings of D. repens infections in German dogs and mosquitoes, strongly suggest that the continuing spread of at least D. repens from its traditional habitats in the Mediterranean has reached southwestern and northeastern Germany.
Climate change with an increase in average temperature may be responsible for propagation of temperature-dependent vectors and/or vector-associated pathogens in regions that were previously not endemic. The analysis of climate data of Brandenburg state (Germany) had showed that the extrinsic development of Dirofilaria repens, the causative agent of canine subcutaneous dirofilariosis, was possible from the years 2001 to 2012. This finding, associated to the movement of infected dogs and their relocation from endemic European areas to Germany makes possible a rapid endemization of the infection and highlight the risk for human health, being D. repens a frequent cause of zoonotic infections.
In Brandenburg, northeastern Germany, an outbreak of zoonotic Dirofilaria repens in a sledge dog kennel was detected in January, 2012. Using the modified Knott test, 8 out of 28 adult dogs were microfilaria positive. A D. repens-specific PCR based on the internal transcribed spacer 2 region detected filarial DNA in 11 of these dogs. Northeastern Germany is currently considered to be free of Dirofilaria. The 39% prevalence within the kennel and the fact that the dogs transiently stayed in endemic areas only during the winter suggest that autochthonous infections occurred. Analysis of weather data shows that extrinsic development of Dirofilaria was continuously possible in the summers of 1994-2012, thus allowing active transmission within the area.
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