Jenny C. Hesson

Global risk model for vector-borne transmission of Zika virus reveals the role of El Niño 2015

Significance This study quantifies the impact of climate variability on Zika virus (ZIKV) transmission by two mosquito vectors with distinct characteristics: Aedes aegypti and Aedes albopictus. Observed climate data were used to dynamically drive a two vectors–one host R0 epidemiological model. Our modeling results indicate that temperature conditions related to the 2015 El Niño climate phenomenon were exceptionally conducive for mosquito-borne transmission of ZIKV over South America. The virus is believed to have entered the continent earlier in 2013. This finding implicates that such a large ZIKV outbreak occurred not solely because of the introduction of ZIKV in a naive population, but because the climatic conditions were optimal for mosquito-borne transmission of ZIKV over South America in 2015. Zika, a mosquito-borne viral disease that emerged in South America in 2015, was declared a Public Health Emergency of International Concern by the WHO in February of 2016. We developed a climate-driven R0 mathematical model for the transmission risk of Zika virus (ZIKV) that explicitly includes two key mosquito vector species: Aedes aegypti and Aedes albopictus. The model was parameterized and calibrated using the most up to date information from the available literature. It was then driven by observed gridded temperature and rainfall datasets for the period 1950–2015. We find that the transmission risk in South America in 2015 was the highest since 1950. This maximum is related to favoring temperature conditions that caused the simulated biting rates to be largest and mosquito mortality rates and extrinsic incubation periods to be smallest in 2015. This event followed the suspected introduction of ZIKV in Brazil in 2013. The ZIKV outbreak in Latin America has very likely been fueled by the 2015–2016 El Niño climate phenomenon affecting the region. The highest transmission risk globally is in South America and tropical countries where Ae. aegypti is abundant. Transmission risk is strongly seasonal in temperate regions where Ae. albopictus is present, with significant risk of ZIKV transmission in the southeastern states of the United States, in southern China, and to a lesser extent, over southern Europe during the boreal summer season.

The arbovirus vector Culex torrentium is more prevalent than Culex pipiens in northern and central Europe

Two species of arbovirus vector, Culex torrentium and Culex pipiens (Diptera: Culicidae), occur in several European countries, but difficulties in their accurate identification and discrimination have hampered both detailed and large‐scale distribution and abundance studies. Using a molecular identification method, we identified to species 2559 larvae of Cx. pipiens/torrentium collected from 138 sites in 13 European countries ranging from Scandinavia to the Mediterranean coast. In addition, samples of 1712 males of Cx. pipiens/torrentium collected at several sites in the Czech Republic were identified to species based on the morphology of their hypopygia. We found that the two species occur together in large areas of Europe, and that Cx. torrentium dominates in northern Europe and Cx. pipiens dominates south of the Alps. The transition in dominance occurs in central Europe, where both species are roughly equally common. There was a strong correlation between the length of the growing season at different sites and occurrences of the two species. As the growing season increases, the proportion and detection of Cx. torrentium decrease, whereas those of Cx. pipiens increase. The present findings have important consequences for the interpretation of the results of studies on major enzootic and link‐vectors of mosquito‐borne bird‐associated viruses (i.e. Sindbis, West Nile and Usutu viruses), especially in central Europe and Scandinavia.

A sensitive and reliable restriction enzyme assay to distinguish between the mosquitoes Culex torrentium and Culex pipiens.

Culex pipiens pipiens Linnaeus and Culex torrentium Martini (Diptera: Culicidae) are closely related vector species that exist sympatrically in Europe. The two species are morphologically almost identical and can only be distinguished with certainty by characters of the male genitalia. Hence, correct species identification and conclusions on distribution and vector status are very difficult and often neglected. Therefore, we developed a reliable and simple mitochondrial cytochrome c oxidase subunit I (COI) gene restriction enzyme assay to discriminate between Cx. pipiens and Cx. torrentium, based on the analysis of morphologically identified male specimens. We sequenced approximately 830 bp in the 3′ region of the mitochondrial COI gene of 18 morphologically identified males of Cx. pipiens and Cx. torrentium. Two restriction enzymes (FspBI and SspI) that could distinguish between the two species according to species‐specific differences in these sequences were chosen. The restriction enzymes were tested on 227 samples from Sweden and verified by sequencing 44 of them. The enzyme FspBI correctly identified all investigated samples; the enzyme SspI identified all samples except one Cx. torrentium. We hope the method and the findings presented here will help to shed light on the true distribution and relative proportions of the two species in Europe.

Geographic Distribution and Relative Abundance of the Sibling Vector Species Culex torrentium and Culex pipiens in Sweden

Culex torrentium and Culex pipiens are sibling species and potential viral vectors that coexist in Europe. Larvae and females of the two species are morphologically almost identical, and reliable identification can only be done on males. To investigate the distribution and relative abundance of the two species in Sweden, we collected Culex larvae from sites spread over the country, identified them as Culex pipiens/torrentium based on morphology, and identified them to species using a recently developed restriction enzyme method. Cx. torrentium was the dominant species (89%, n=1012) and it occurred in 48 of the 49 sites investigated, and also dominated in most of the study sites. The proportion of Cx. pipiens larvae in relation to Cx. torrentium collected at each site decreased with both increasing latitude and altitude, and the presence of Cx. pipiens decreased with latitude. In addition, Cx. pipiens/torrentium females were sampled with Centres for Disease Control light traps baited with carbon dioxide. The overall country mean was 4.0 Cx. pipiens/torrentium caught per trap night, with decreasing numbers of Cx. pipiens/torrentium caught per trap night with increasing latitude. Thus, the abundance of Cx. pipiens/torrentium decreased, but the proportion Cx. torrentium increased, with increasing latitude. This is the first study that shows the vast dominance of Cx. torrentium over Cx. pipiens in Sweden. The unexpected dominance of Cx. torrentium highlights the importance of distinguishing between the two species in studies of Culex-borne arboviruses in Europe.

Culex torrentium Mosquito Role as Major Enzootic Vector Defined by Rate of Sindbis Virus Infection, Sweden, 2009

We isolated Sindbis virus (SINV) from the enzootic mosquito vectors Culex torrentium, Cx. pipiens, and Culiseta morsitans collected in an area of Sweden where SINV disease is endemic. The infection rate in Cx. torrentium mosquitoes was exceptionally high (36 infections/1,000 mosquitoes), defining Cx. torrentium as the main enzootic vector of SINV in Scandinavia.

Trapping Biases of Culex torrentium and Culex pipiens Revealed by Comparison of Captures in CDC Traps, Ovitraps, and Gravid Traps

ABSTRACT: We evaluate three trapping methods for their effectiveness at capturing Culex pipiens and Culex torrentium, both enzootic vectors of bird-associated viruses in Europe. The comparisons, performed in two regions in Sweden, were among CDC traps baited with carbon dioxide, gravid traps, and ovitraps baited with hay infusion. The proportions of the two Culex species in a catch differed between trap types, with CDC traps catching a lower proportion of Cx. torrentium than both gravid traps and ovitraps. Between gravid traps and ovitraps, there was no difference in the proportions of the two species. The results indicate that Cx. torrentium may go undetected or underestimated compared to Cx. pipiens when using carbon dioxide baited CDC traps. The new insight of trap bias presented here adds an important dimension to consider when investigating these vectors of bird-associated viruses in the field.

First report on human-biting Culex pipiens in Sweden

Culex mosquitoes are vectors of several bird-hosted arboviruses that cause outbreaks in Europe, such as Sindbis virus and West Nile virus. Recently, the human-biting form of Culex pipiens, Cx. pipiens biotype molestus, was found causing big nuisance in a housing cooperative in Gothenburg in southern Sweden, confirmed by molecular identification. This is the first report of human-biting Culex in Scandinavia, signalling increased risk of arbovirus infection in northern Europe.

Temporal Variation in Sindbis Virus Antibody Prevalence in Bird Hosts in an Endemic Area in Sweden.

Sindbis virus (SINV) is a mosquito-borne bird virus that occasionally causes human disease in Fennoscandia, suggested to have cyclic 7-year intervals between outbreaks. Reliable data on human infections in Sweden is however lacking. Here we investigated the SINV antibody prevalence among birds in a Swedish area endemic to SINV to scrutinize if a cyclic variation in antibody prevalence is present in the natural host of SINV. Serum from birds were sampled in the summers of 2002–2004 and 2009 in the floodplains of the River Dalälven in central Sweden, with 2002 and 2009 representing hypothesized years of SINV outbreaks. A total of 963 birds from 52 species (mainly passerines) were tested for the presence of SINV antibodies using a plaque reduction neutralization test. The highest SINV antibody prevalence was found in Turdidae species, specifically Fieldfare, Redwing and Song thrush in which more than 70% of sampled individuals had antibodies to SINV in 2009. The SINV antibody prevalence significantly varied between years with 2% in 2002, 8% in 2003, 14% in 2004 and 37% in 2009. Antibodies were found equally often in hatchlings and in adults and increased from early to late in the season. Clearly, the SINV antibody prevalence was not elevated in the bird hosts in the predicted outbreak year 2002, thus solid evidence of a cyclic occurrence of SINV in Sweden is still lacking.

Pest occurrence of Aedes rossicus close to the Arctic Circle in northern Sweden

ABSTRACT: Major nuisance species are found among the floodwater mosquitoes and snow-pool mosquitoes, with the former being the main reason for mosquito control in most areas. Nuisance species vary with the area, and previous reports from northern areas conclude that the nuisance is most often caused by snow-pool mosquitoes. We investigated the mosquito fauna and abundances of host-seeking females using CDC traps baited with carbon dioxide, in Övertorneå city near the Arctic Circle in northern Sweden, after earlier complaints about massive mosquito nuisance. The abundance of host-seeking female mosquitoes was high in 2014, with a maximum of ~15,400 individuals per CDC trap night, of which 89% was the floodwater mosquito Aedes rossicus. Surprisingly, the main nuisance species was a floodwater mosquito, occurring at the northernmost location it has ever been recorded in Sweden. Our report is probably the first documentation of such large numbers of Aedes rossicus in any locality and probably the first documentation of a severe floodwater mosquito nuisance near the Arctic Circle. Given the historical data on river discharge in the area, the nuisance is recurrent. We conclude that in northern localities, as well as in more southern localities, production of floodwater mosquitoes is a natural component of the floodplain fauna of rivers with a fluctuating water flow regime. Also, the floodwater mosquitoes Aedes sticticus and Aedes vexans were found north of their formerly known distribution in Sweden.