Reconstructing the recent West Nile virus lineage 2 epidemic in Europe and Italy using discrete and continuous phylogeography

Zehender, Gianguglielmo; Veo, Carla; Ebranati, Erika; Carta, Valentina; Rovida, Francesca; Percivalle, Elena; Moreno, Ana; Lelli, Davide; Calzolari, Mattia; Llombart‐Bosch, Antonio; Chiapponi, Chiara; Baioni, Laura; Capelli, Gioia; Ravagnan, Silvia; Rold, Graziana Da; Lavezzo, Enrico; Palù, Giorgio; Baldanti, Fausto; Barzon, Luisa; Galli, Massimo

doi:10.1371/journal.pone.0179679

Cited by 55 publications

(59 citation statements)

References 44 publications

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“…These results were confirmed by the East–West geographical shift observed when plotting the cumulative distribution curves of WNND cases by longitude. Interestingly, similar results have been found by a phylogenetic analysis conducted among humans, mosquitoes and birds, which underlined that the WNV spatial spread observed in Northern Italy in recent years probably occurred along the Po river and its main tributaries with an East–West gradient (Zehender et al, ). These results suggest that Po River and its neighbouring areas might present environmental and ecological conditions that can promote WNV transmission and circulation.…”

Section: Discussionsupporting

confidence: 76%

“…Once introduced in new areas by infected migratory birds, WNV must establish an endemic cycle of transmission among immunologically naïve birds and mosquitoes (Chancey et al, ). It has been shown that the virus can circulate among reservoirs and vectors for several years before causing significant human outbreaks (Zehender et al, ). It has been hypothesized that the persistence of the virus in new affected areas might be due to infected birds that develop persistent WNV infection.…”

Section: Discussionmentioning

confidence: 99%

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Recent rapid changes in the spatio‐temporal distribution of West Nile Neuro‐invasive Disease in Italy

Moirano

Richiardi

Calzolari

et al. 2019

Zoonoses and Public Health

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In Italy, the first human case of West Nile Virus (WNV) infection was reported in 2008 and, since then, the number of cases has been steadily increasing. In this study, we describe the temporal and spatial pattern of WNV infection risk among humans in Italy, focusing on the human cases of West Nile Neuro‐invasive Disease (WNND) observed between 2008 and 2017. Incidence rates are estimated for each year and province under study. The incidence temporal trend is estimated using Poisson regression, and a spatio‐temporal cluster detection analysis is performed to detect high‐risk areas. In total, 231 WNND cases were notified in Italy between 2008 and 2017. The annual incidence rates increased during the study period (annual percentage change: 11.7%; 95%CI: −0.9%; 26.1%). A geographical spread of the disease was observed during the study period throughout Northern Italy, with an increasing number of affected provinces. Provinces close to the Po River (the main river in the north of Italy) and the Oristano province (in the Sardinia Island) experienced the highest incidence rates during the study period. Our study shows a gradual, but rapid spread of WNND across Northern Italy from east to west and suggests the hypothesis that provinces close to Po River might present ecological and climatic conditions favourable to the virus circulation.

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Section: Discussionsupporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Recent rapid changes in the spatio‐temporal distribution of West Nile Neuro‐invasive Disease in Italy

Moirano

Richiardi

Calzolari

et al. 2019

Zoonoses and Public Health

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“…Furthermore, in this country, significant seroprevalence levels have recently been described in humans with meningitis and lymphocytic meningitis (14 of 42 cases), as well as in horses and wild birds [44]. Finally, as suggested by Zehender et al [61], WNV may need a few years of enzootic circulation before transmission to dead-end hosts: Poland may be in this situation. This time lag may be partially explained by the above–mentioned conjectural risk and justify a long term surveillance and awareness in risky areas.…”

Section: Discussionmentioning

confidence: 99%

Geographic variations of the bird-borne structural risk of West Nile virus circulation in Europe

et al. 2017

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The structural risk of West Nile Disease results from the usual functioning of the socio-ecological system, which may favour the introduction of the pathogen, its circulation and the occurrence of disease cases. Its geographic variations result from the local interactions between three components: (i) reservoir hosts, (ii) vectors, both characterized by their diversity, abundance and competence, (iii) and the socio-economic context that impacts the exposure of human to infectious bites. We developed a model of bird-borne structural risk of West Nile Virus (WNV) circulation in Europe, and analysed the association between the geographic variations of this risk and the occurrence of WND human cases between 2002 and 2014. A meta-analysis of WNV serosurveys conducted in wild bird populations was performed to elaborate a model of WNV seropositivity in European bird species, considered a proxy for bird exposure to WNV. Several eco-ethological traits of bird species were linked to seropositivity and the statistical model adequately fitted species-specific seropositivity data (area under the ROC curve: 0.85). Combined with species distribution maps, this model allowed deriving geographic variations of the bird-borne structural risk of WNV circulation. The association between this risk, and the occurrence of WND human cases across the European Union was assessed. Geographic risk variations of bird-borne structural risk allowed predicting WND case occurrence in administrative districts of the EU with a sensitivity of 86% (95% CI: 0.79–0.92), and a specificity of 68% (95% CI: 0.66–0.71). Disentangling structural and conjectural health risks is important for public health managers as risk mitigation procedures differ according to risk type. The results obtained show promise for the prevention of WND in Europe. Combined with analyses of vector-borne structural risk, they should allow designing efficient and targeted prevention measures.

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“…The d N /d S ratios for all genes in WNV-2 Europe are higher than those in WNV-1 except NS4A and also those in WNV-2 Africa except NS5, suggesting that WNV-2 European has a smaller N e than WNV-1 and WNV-2 Africa and/or the effect of negative selection has not been fully accumulated (rule 5). Note that WNV-2 Europe is likely a young strain, as it was transmitted to Europe probably in early 21st century (24).…”

Section: Significancementioning

confidence: 99%

Many human RNA viruses show extraordinarily stringent selective constraints on protein evolution

Lin

Bhattacharjee

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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How negative selection, positive selection, and population size contribute to the large variation in nucleotide substitution rates among RNA viruses remains unclear. Here, we studied the ratios of nonsynonymous-to-synonymous substitution rates (d N /d S ) in proteincoding genes of human RNA and DNA viruses and mammals. Among the 21 RNA viruses studied, 18 showed a genome-average d N /d S from 0.01 to 0.10, indicating that over 90% of nonsynonymous mutations are eliminated by negative selection. Only HIV-1 showed a d N /d S (0.31) higher than that (0.22) in mammalian genes. By comparing the d N /d S values among genes in the same genome and among species or strains, we found that both positive selection and population size play significant roles in the d N /d S variation among genes and species. Indeed, even in flaviviruses and picornaviruses, which showed the lowest ratios among the 21 species studied, positive selection appears to have contributed significantly to d N /d S . We found the view that positive selection occurs much more frequently in influenza A subtype H3N2 than subtype H1N1 holds only for the hemagglutinin and neuraminidase genes, but not for other genes. Moreover, we found no support for the view that vector-borne RNA viruses have lower d N /d S ratios than non-vector-borne viruses. In addition, we found a correlation between d N and d S , implying a correlation between d N and the mutation rate. Interestingly, only 2 of the 8 DNA viruses studied showed a d N /d S < 0.10, while 4 showed a d N /d S > 0.22. These observations increase our understanding of the mechanisms of RNA virus evolution. picornaviruses | flaviviruses | influenza A viruses | selective constraints | positive selection R ates of nucleotide substitution can be up to 1 million-fold higher in RNA viruses than in their cellular hosts (1-3). This rapid evolution is mainly due to high mutation rates (4, 5), while natural selection occurs mostly as purifying selection (5, 6). Selection is usually measured by the d N /d S ratio, where d S (d N ) is the number of synonymous (nonsynonymous) substitutions per synonymous (nonsynonymous) site between 2 sequences. Although d N /d S has been studied in many RNA viruses (7), some important issues remain unresolved. One question is the relative contributions of natural selection and effective population size (N e ) to differences in d N /d S among viral species. Positive (Darwinian) selection increases, while negative (purifying) selection decreases, d N /d S . Unfortunately, it is difficult to determine whether an instance of elevated d N /d S is due to positive selection or relaxed negative selection. Positive selection has been found in viruses such as influenza A viruses (8,9) and HIV-1 (10-12). However, the contribution of positive selection to the genomic mean d N /d S has not been evaluated. Because natural selection is more effective in large populations and negative selection predominates (7), an increase in N e would be expected to reduce the mean d N /d S . Unfortunately, N e is usual...

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Reconstructing the recent West Nile virus lineage 2 epidemic in Europe and Italy using discrete and continuous phylogeography

Cited by 55 publications

References 44 publications

Recent rapid changes in the spatio‐temporal distribution of West Nile Neuro‐invasive Disease in Italy

Recent rapid changes in the spatio‐temporal distribution of West Nile Neuro‐invasive Disease in Italy

Geographic variations of the bird-borne structural risk of West Nile virus circulation in Europe

Many human RNA viruses show extraordinarily stringent selective constraints on protein evolution

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