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1.  Early warning of West Nile virus mosquito vector: climate and land use models successfully explain phenology and abundance of Culex pipiens mosquitoes in north-western Italy 
Parasites & Vectors  2014;7:269.
West Nile Virus (WNV) is an emerging global health threat. Transmission risk is strongly related to the abundance of mosquito vectors, typically Culex pipiens in Europe. Early-warning predictors of mosquito population dynamics would therefore help guide entomological surveillance and thereby facilitate early warnings of transmission risk.
We analysed an 11-year time series (2001 to 2011) of Cx. pipiens mosquito captures from the Piedmont region of north-western Italy to determine the principal drivers of mosquito population dynamics. Linear mixed models were implemented to examine the relationship between Cx. pipiens population dynamics and environmental predictors including temperature, precipitation, Normalized Difference Water Index (NDWI) and the proximity of mosquito traps to urban areas and rice fields.
Warm temperatures early in the year were associated with an earlier start to the mosquito season and increased season length, and later in the year, with decreased abundance. Early precipitation delayed the start and shortened the length of the mosquito season, but increased total abundance. Conversely, precipitation later in the year was associated with a longer season. Finally, higher NDWI early in the year was associated with an earlier start to the season and increased season length, but was not associated with abundance. Proximity to rice fields predicted higher total abundance when included in some models, but was not a significant predictor of phenology. Proximity to urban areas was not a significant predictor in any of our models. Predicted variations in start of the season and season length ranged from one to three weeks, across the measured range of variables. Predicted mosquito abundance was highly variable, with numbers in excess of 1000 per trap per year when late season temperatures were low (average 21°C) to only 150 when late season temperatures were high (average 30°C).
Climate data collected early in the year, in conjunction with local land use, can be used to provide early warning of both the timing and magnitude of mosquito outbreaks. This potentially allows targeted mosquito control measures to be implemented, with implications for prevention and control of West Nile Virus and other mosquito borne diseases.
PMCID: PMC4061321  PMID: 24924622
Culex pipiens; Population dynamics; Epidemiology; Linear-mixed models; Remote sensing
2.  Lack of identification of Flaviviruses in oral and cloacal swabs from long- and short-distance migratory birds in Trentino-Alto Adige (North-eastern Italy) 
Virology Journal  2013;10:306.
West Nile virus (WNV) and Usutu virus (USUV), both belonging to the genus Flavivirus, are emerging in Italy as important human and animal pathogens. Migratory birds are involved in the spread of Flaviviruses over long distances, particularly from Africa to Europe. Once introduced, these viruses can be further be dispersed by short-distance migratory and resident bird species. Thus far, there is still a considerable knowledge gap on the role played by different bird species in the ecology and transmission mechanisms of these viruses. The Region of Trentino-Alto Adige (north-eastern Italy) is located on the migratory route of many of the short- and long-distance migratory birds that cross the Alps, connecting northern Europe and western Asia with southern Europe and Africa. Until now, only a silent circulation of WNV and USUV within the territory of the Province of Trento has been confirmed by serological screening, whilst no cases of infected humans or animals have so far been reported. However, continuous spillover events of both viruses have been reported in neighbouring Regions. The aim of this study was to monitor the circulation of WNV and USUV in Trentino-Alto Adige, in order to detect if active virus shedding occurs in migratory birds captured during their seasonal movements and to evaluate the role that different bird species could play in the spreading of these viruses.
We carried out a biomolecular survey on oral and cloacal swabs collected from migratory birds during seasonal migrations. Birds belonging to 18 transaharian and 21 intrapaleartic species were examined during spring (n = 176) and autumn (n = 146), and were tested using a generic nested-PCR.
All samples tested negative for Flaviviruses. The possible causes of unapparent shedding, along with ecological and epidemiological implications are discussed.
The lack of detection of active virus shedding in these bird species does not exclude the circulation of these viruses within the Trentino-Alto Adige region, as reported in previous studies. The possible ecological implications are discussed.
PMCID: PMC3852823  PMID: 24119320
Flavivirus; Migratory birds; Oral and cloacal swabs; Survey
3.  Small ruminant macrophage polarization may play a pivotal role on lentiviral infection 
Veterinary Research  2013;44(1):83.
Small ruminant lentiviruses (SRLV) infect the monocyte/macrophage lineage inducing a long-lasting infection affecting body condition, production and welfare of sheep and goats all over the world. Macrophages play a pivotal role on the host’s innate and adaptative immune responses against parasites by becoming differentially activated. Macrophage heterogeneity can tentatively be classified into classically differentiated macrophages (M1) through stimulation with IFN-γ displaying an inflammatory profile, or can be alternatively differentiated by stimulation with IL-4/IL-13 into M2 macrophages with homeostatic functions. Since infection by SRLV can modulate macrophage functions we explored here whether ovine and caprine macrophages can be segregated into M1 and M2 populations and whether this differential polarization represents differential susceptibility to SRLV infection. We found that like in human and mouse systems, ovine and caprine macrophages can be differentiated with particular stimuli into M1/M2 subpopulations displaying specific markers. In addition, small ruminant macrophages are plastic since M1 differentiated macrophages can express M2 markers when the stimulus changes from IFN-γ to IL-4. SRLV replication was restricted in M1 macrophages and increased in M2 differentiated macrophages respectively according to viral production. Identification of the infection pathways in macrophage populations may provide new targets for eliciting appropriate immune responses against SRLV infection.
PMCID: PMC3850683  PMID: 24070317
4.  Evidence of mosquito-transmitted flavivirus circulation in Piedmont, north-western Italy 
Parasites & Vectors  2012;5:99.
Flavivirus is a highly heterogeneous viral genus that includes important human pathogens and several viral strains with unknown zoonotic potential. Mosquito-borne flaviviruses have been isolated and characterized in Northern Italy: West Nile virus and Usutu virus were detected in mosquitoes and in different host species and recent studies provided evidence about the circulation of “insect Flavivirus” strains.
In order to clarify the diffusion and the distribution of the mosquito-transmitted flaviviruses in Italy, we analyzed Culex and Ochlerotatus mosquitoes collected in 2009 and 2010 in an area divided evenly between hills and plains and where the landscape is dominated by mixed agricultural patches, rice fields, deciduous tree forests, and urban environments. Each mosquito pool was tested for the presence of Flavivirus strains and we characterized positive samples by genetic sequencing.
Positive mosquito pools revealed low infection prevalence, but suggested a continuous circulation of both Usutu virus and insect Flavivirus. Interestingly, phylogenetic analyses based on NS5 gene partial sequences showed a closer relationship among new Usutu virus strains from Piedmont and the reference sequences from the Eastern Europe, with respect to Italian samples characterized so far. Moreover, NS5 gene phylogeny suggested that mosquito flaviviruses found in Italy could belong to different lineages.
Our results contribute to a wider point of view on the heterogeneity of viruses infecting mosquitoes suggesting a taxonomical revision of the Mosquito-borne Flavivirus group.
PMCID: PMC3407742  PMID: 22616748
Usutu virus; Insect Flavivirus; Culex pipiens; Ochlerotatus caspius
5.  Study of compartmentalization in the visna clinical form of small ruminant lentivirus infection in sheep 
A central nervous system (CNS) disease outbreak caused by small ruminant lentiviruses (SRLV) has triggered interest in Spain due to the rapid onset of clinical signs and relevant production losses. In a previous study on this outbreak, the role of LTR in tropism was unclear and env encoded sequences, likely involved in tropism, were not investigated. This study aimed to analyze heterogeneity of SRLV Env regions - TM amino terminal and SU V4, C4 and V5 segments - in order to assess virus compartmentalization in CNS.
Eight Visna (neurologically) affected sheep of the outbreak were used. Of the 350 clones obtained after PCR amplification, 142 corresponded to CNS samples (spinal cord and choroid plexus) and the remaining to mammary gland, blood cells, bronchoalveolar lavage cells and/or lung. The diversity of the env sequences from CNS was 11.1-16.1% between animals and 0.35-11.6% within each animal, except in one animal presenting two sequence types (30% diversity) in the CNS (one grouping with those of the outbreak), indicative of CNS virus sequence heterogeneity. Outbreak sequences were of genotype A, clustering per animal and compartmentalizing in the animal tissues. No CNS specific signature patterns were found.
Bayesian approach inferences suggested that proviruses from broncoalveolar lavage cells and peripheral blood mononuclear cells represented the common ancestors (infecting viruses) in the animal and that neuroinvasion in the outbreak involved microevolution after initial infection with an A-type strain. This study demonstrates virus compartmentalization in the CNS and other body tissues in sheep presenting the neurological form of SRLV infection.
PMCID: PMC3328241  PMID: 22281181
Compartmentalization; Visna; Small ruminant lentivirus; Spinal cord; Choroid plexus; Sheep
6.  Spatio-temporal patterns of distribution of West Nile virus vectors in eastern Piedmont Region, Italy 
Parasites & Vectors  2011;4:230.
West Nile Virus (WNV) transmission in Italy was first reported in 1998 as an equine outbreak near the swamps of Padule di Fucecchio, Tuscany. No other cases were identified during the following decade until 2008, when horse and human outbreaks were reported in Emilia Romagna, North Italy. Since then, WNV outbreaks have occurred annually, spreading from their initial northern foci throughout the country. Following the outbreak in 1998 the Italian public health authority defined a surveillance plan to detect WNV circulation in birds, horses and mosquitoes. By applying spatial statistical analysis (spatial point pattern analysis) and models (Bayesian GLMM models) to a longitudinal dataset on the abundance of the three putative WNV vectors [Ochlerotatus caspius (Pallas 1771), Culex pipiens (Linnaeus 1758) and Culex modestus (Ficalbi 1890)] in eastern Piedmont, we quantified their abundance and distribution in space and time and generated prediction maps outlining the areas with the highest vector productivity and potential for WNV introduction and amplification.
The highest abundance and significant spatial clusters of Oc. caspius and Cx. modestus were in proximity to rice fields, and for Cx. pipiens, in proximity to highly populated urban areas. The GLMM model showed the importance of weather conditions and environmental factors in predicting mosquito abundance. Distance from the preferential breeding sites and elevation were negatively associated with the number of collected mosquitoes. The Normalized Difference Vegetation Index (NDVI) was positively correlated with mosquito abundance in rice fields (Oc. caspius and Cx. modestus). Based on the best models, we developed prediction maps for the year 2010 outlining the areas where high abundance of vectors could favour the introduction and amplification of WNV.
Our findings provide useful information for surveillance activities aiming to identify locations where the potential for WNV introduction and local transmission are highest. Such information can be used by vector control offices to stratify control interventions in areas prone to the invasion of WNV and other mosquito-transmitted pathogens.
PMCID: PMC3251540  PMID: 22152822
7.  Taxon ordering in phylogenetic trees by means of evolutionary algorithms 
BioData Mining  2011;4:20.
In in a typical "left-to-right" phylogenetic tree, the vertical order of taxa is meaningless, as only the branch path between them reflects their degree of similarity. To make unresolved trees more informative, here we propose an innovative Evolutionary Algorithm (EA) method to search the best graphical representation of unresolved trees, in order to give a biological meaning to the vertical order of taxa.
Starting from a West Nile virus phylogenetic tree, in a (1 + 1)-EA we evolved it by randomly rotating the internal nodes and selecting the tree with better fitness every generation. The fitness is a sum of genetic distances between the considered taxon and the r (radius) next taxa. After having set the radius to the best performance, we evolved the trees with (λ + μ)-EAs to study the influence of population on the algorithm.
The (1 + 1)-EA consistently outperformed a random search, and better results were obtained setting the radius to 8. The (λ + μ)-EAs performed as well as the (1 + 1), except the larger population (1000 + 1000).
The trees after the evolution showed an improvement both of the fitness (based on a genetic distance matrix, then close taxa are actually genetically close), and of the biological interpretation. Samples collected in the same state or year moved close each other, making the tree easier to interpret. Biological relationships between samples are also easier to observe.
PMCID: PMC3142222  PMID: 21718550
8.  Multi-year evolutionary dynamics of West Nile virus in suburban Chicago, USA, 2005–2007 
West Nile virus has evolved in concert with its expansion across North America, but little is known about the evolutionary dynamics of the virus on local scales. We analysed viral nucleotide sequences from mosquitoes collected in 2005, 2006, and 2007 from a known transmission ‘hot spot’ in suburban Chicago, USA. Within this approximately 11 × 14 km area, the viral envelope gene has increased approximately 0.1% yr−1 in nucleotide-level genetic diversity. In each year, viral diversity was higher in ‘residential’ sites characterized by dense housing than in more open ‘urban green space’ sites such as cemeteries and parks. Phylodynamic analyses showed an increase in incidence around 2005, consistent with a higher-than-average peak in mosquito and human infection rates that year. Analyses of times to most recent common ancestor suggest that WNV in 2005 and 2006 may have arisen predominantly from viruses present during 2004 and 2005, respectively, but that WNV in 2007 had an older common ancestor, perhaps indicating a predominantly mixed or exogenous origin. These results show that the population of WNV in suburban Chicago is an admixture of viruses that are both locally derived and introduced from elsewhere, containing evolutionary information aggregated across a breadth of spatial and temporal scales.
PMCID: PMC2880109  PMID: 20478882
West Nile virus; evolution; ecology; phylogenetics; phylodynamics
9.  Taxon ordering in phylogenetic trees: a workbench test 
BMC Bioinformatics  2011;12:58.
Phylogenetic trees are an important tool for representing evolutionary relationships among organisms. In a phylogram or chronogram, the ordering of taxa is not considered meaningful, since complete topological information is given by the branching order and length of the branches, which are represented in the root-to-node direction. We apply a novel method based on a (λ + μ)-Evolutionary Algorithm to give meaning to the order of taxa in a phylogeny. This method applies random swaps between two taxa connected to the same node, without changing the topology of the tree. The evaluation of a new tree is based on different distance matrices, representing non-phylogenetic information such as other types of genetic distance, geographic distance, or combinations of these. To test our method we use published trees of Vesicular stomatitis virus, West Nile virus and Rice yellow mottle virus.
Best results were obtained when taxa were reordered using geographic information. Information supporting phylogeographic analysis was recovered in the optimized tree, as evidenced by clustering of geographically close samples. Improving the trees using a separate genetic distance matrix altered the ordering of taxa, but not topology, moving the longest branches to the extremities, as would be expected since they are the most divergent lineages. Improved representations of genetic and geographic relationships between samples were also obtained when merged matrices (genetic and geographic information in one matrix) were used.
Our innovative method makes phylogenetic trees easier to interpret, adding meaning to the taxon order and helping to prevent misinterpretations.
PMCID: PMC3050728  PMID: 21352514
10.  Modeling the Spread of Vector-Borne Diseases on Bipartite Networks 
PLoS ONE  2010;5(11):e13796.
Vector-borne diseases for which transmission occurs exclusively between vectors and hosts can be modeled as spreading on a bipartite network.
Methodology/Principal Findings
In such models the spreading of the disease strongly depends on the degree distribution of the two classes of nodes. It is sufficient for one of the classes to have a scale-free degree distribution with a slow enough decay for the network to have asymptotically vanishing epidemic threshold. Data on the distribution of Ixodes ricinus ticks on mice and lizards from two independent studies are well described by a scale-free distribution compatible with an asymptotically vanishing epidemic threshold. The commonly used negative binomial, instead, cannot describe the right tail of the empirical distribution.
The extreme aggregation of vectors on hosts, described by the power-law decay of the degree distribution, makes the epidemic threshold decrease with the size of the network and vanish asymptotically.
PMCID: PMC2980486  PMID: 21103064
11.  Evolutionary Dynamics of Multiple Sublineages of H5N1 Influenza Viruses in Nigeria from 2006 to 2008 ▿ †  
Journal of Virology  2010;84(7):3239-3247.
Highly pathogenic A/H5N1 avian influenza (HPAI H5N1) viruses have seriously affected the Nigerian poultry industry since early 2006. Previous studies have identified multiple introductions of the virus into Nigeria and several reassortment events between cocirculating lineages. To determine the spatial, evolutionary, and population dynamics of the multiple H5N1 lineages cocirculating in Nigeria, we conducted a phylogenetic analysis of whole-genome sequences from 106 HPAI H5N1 viruses isolated between 2006 and 2008 and representing all 25 Nigerian states and the Federal Capital Territory (FCT) reporting outbreaks. We identified a major new subclade in Nigeria that is phylogenetically distinguishable from all previously identified sublineages, as well as two novel reassortment events. A detailed analysis of viral phylogeography identified two major source populations for the HPAI H5N1 virus in Nigeria, one in a major commercial poultry area (southwest region) and one in northern Nigeria, where contact between wild birds and backyard poultry is frequent. These findings suggested that migratory birds from Eastern Europe or Russia may serve an important role in the introduction of HPAI H5N1 viruses into Nigeria, although virus spread through the movement of poultry and poultry products cannot be excluded. Our study provides new insight into the genesis and evolution of H5N1 influenza viruses in Nigeria and has important implications for targeting surveillance efforts to rapidly identify the spread of the virus into and within Nigeria.
PMCID: PMC2838112  PMID: 20071565
12.  Genome Analysis of Small-Ruminant Lentivirus Genotype E: a Caprine Lentivirus with Natural Deletions of the dUTPase Subunit, vpr-Like Accessory Gene, and 70-Base-Pair Repeat of the U3 Region ▿  
Journal of Virology  2008;83(2):1152-1155.
The nucleotide sequence of the highly divergent small-ruminant lentivirus genotype E has been determined. The full genome consists of 8,418 nucleotides and lacks two large portions corresponding nearly to the entire dUTPase subunit of the pol and vpr-like accessory genes. Moreover, the 70-bp repeat of the U3 region of the long terminal repeat was observed to be deleted. Interestingly, this lentivirus genotype is able to persist in a local breed population, and retrospective analysis revealed its presence in milk samples collected in 1999. gag sequences obtained from a flock coinfected with the B1 and E genotypes revealed that the evolutionary rates of the two viruses were quite similar. Since a reduced viral load and/or disease progression was observed for viruses with artificially deleted dUTPase and vpr-like genes, it is proposed that this viral cluster be designated a low-pathogenicity caprine lentivirus.
PMCID: PMC2612395  PMID: 18987157
13.  Rickettsia slovaca in Dermacentor marginatus and Tick-borne Lymphadenopathy, Tuscany, Italy 
Emerging Infectious Diseases  2008;14(5):817-820.
Of 263 patients in Tuscany, Italy, from whom ticks were removed during July 2005–May 2007, five showed signs of tick-borne encephalopathy. Of the ticks, 17 were Dermacentor marginatus; 6 (35.3%) of these were identified by sequence analysis as containing Rickettsia slovaca. Tick-borne lympadenopathy occurs in this area.
PMCID: PMC2600248  PMID: 18439371
Tick-borne lympadenopathy; Rickettsia slovaca; Dermacentor marginatus; surveillance system; dispatch

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