Next Article in Journal
Bridging the Gaps: Investigating the Complex Impact of the COVID-19 Pandemic on Tuberculosis Records in Brazil
Previous Article in Journal
Seroprevalence of Crimean Congo Hemorrhagic Fever Virus in Occupational Settings: Systematic Review and Meta-Analysis
Previous Article in Special Issue
In Silico Analysis Reveals High Levels of Genetic Diversity of Plasmodium knowlesi Cell Traversal Protein for Ookinetes and Sporozoites (PkCelTOS) in Clinical Samples
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
TropicalMed
Volume 8
Issue 9
10.3390/tropicalmed8090453
tropicalmed-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Ongoing Epidemic of West Nile Virus in Greece: The Contribution of Biological Vectors and Reservoirs and the Importance of Climate and Socioeconomic Factors Revisited

by
Dimitrios Kouroupis
1,
Konstantina Charisi
2 and
Athina Pyrpasopoulou
1,2,*
1
2nd Propedeutic Department of Internal Medicine, Hippokration Hospital, Konstantinoupoleos 49, 54642 Thessaloniki, Greece
2
Infectious Diseases Unit, Hippokration Hospital, Konstantinoupoleos 49, 54642 Thessaloniki, Greece
*
Author to whom correspondence should be addressed.
Trop. Med. Infect. Dis. 2023, 8(9), 453; https://doi.org/10.3390/tropicalmed8090453
Submission received: 30 August 2023 / Revised: 17 September 2023 / Accepted: 17 September 2023 / Published: 19 September 2023
(This article belongs to the Special Issue Emerging Vector-Borne Diseases and Public Health Challenges)
Browse Figures
Versions Notes

Abstract

:
Emerging infectious diseases have inflicted a significant health and socioeconomic burden upon the global population and governments worldwide. West Nile virus, a zoonotic, mosquito-borne flavivirus, was originally isolated in 1937 from a febrile patient in the West Nile Province of Uganda. It remained confined mainly to Africa, the Middle East, and parts of Europe and Australia until 1999, circulating in an enzootic mosquito-bird transmission cycle. Since the beginning of the 21st century, a new, neurotropic, more virulent strain was isolated from human outbreaks initially occurring in North America and later expanding to South and South-eastern Europe. Since 2010, when the first epidemic was recorded in Greece, annual incidence has fluctuated significantly. A variety of environmental, biological and socioeconomic factors have been globally addressed as potential regulators of the anticipated intensity of the annual incidence rate; circulation within the zoonotic reservoirs, recruitment and adaptation of new potent arthropod vectors, average winter and summer temperatures, precipitation during the early summer months, and socioeconomic factors, such as the emergence and progression of urbanization and the development of densely populated areas in association with insufficient health policy measures. This paper presents a review of the biological and socioenvironmental factors influencing the dynamics of the epidemics of West Nile virus (WNV) cases in Greece, one of the highest-ranked European countries in terms of annual incidence. To date, WNV remains an unpredictable opponent as is also the case with other emerging infectious diseases, forcing the National Health systems to develop response strategies, control the number of infections, and shorten the duration of the epidemics, thus minimizing the impact on human and material resources.

1. West Nile Virus: Pathogenicity and Virulence

West Nile virus (WNV), is a positive-stranded ribonucleic acid (RNA) virus. It belongs to the family of Flaviviridae, in the Japanese encephalitis antigenic complex [1]. Other members of the family include Zika virus, Dengue virus, and Yellow Fever virus. West Nile virions are ~50 nm in diameter with icosahedral symmetry and consist of a spherical nucleocapsid surrounded by an envelope [2].
WNV was first isolated in 1937 from a woman in the West Nile district in Uganda [3]. In the 77 years since its discovery, the virus has expanded to a vast region of the globe, in parts of North and South America, Africa, Europe, Asia, and Oceania, and is now considered the most important causative agent of viral encephalitis worldwide [4].
Eight phylogenetic lineages have been described, but only lineages 1 and 2 are associated with disease in humans. Lineage 1 and its multiple profiles are the source of the epidemic transmission in Africa and throughout the world. Lineage 2 was considered an African zoonosis and has historically been considered to be less pathogenic in humans than lineage 1. However, in 2004, lineage 2, previously only isolated from horses in sub-Saharan Africa and Madagascar, appeared in Hungary, where the first recorded outbreak affected 18 horses. Prior to the emergence of a lineage 2 strain in Hungary in 2004, sporadic cases and occasional outbreaks in animals and humans in Europe were linked to lineage 1 strains. Since 2008, the lineage 2 strain has spread over central Europe and the eastern Mediterranean region and has become more virulent in vertebrates [5]. This strain, although not previously considered to be of public health importance, appears to have evolved into a more virulent phenotype and has since caused significant outbreaks in humans and animals in several countries, including Greece, Hungary, and Serbia [6]. A discrete lineage 2 virus emerged in southern Russia in 2007, which spread to Romania and Italy after 2010.
The significant majority of WNV infections in humans are asymptomatic. About 20–25% of WNV infections may cause a mild disease, associated with a wide variety of symptoms [7]. Neuroinvasive disease (meningitis, encephalitis, acute flaccid paralysis), although very rare, occurring in <1% of the infected patients, is characterised by significant mortality (~10%) and long-term morbidity [8] and occurs more readily in aged and immunocompromised patients.
Infection is initiated after the vector salivary components are introduced into keratinocytes and skin dendritic cells and/or macrophages. The inflammatory response that follows leads to the recruitment of neutrophils, which secrete attractants to summon monocytes. The monocytes are differentiated into dendritic cells and macrophages and become attacked by the virus, while in the meantime, the resident dermal dendritic cells migrate to draining lymph nodes to induce adaptive immunity [9]. In the cases of neuroinvasive disease, the virus is considered to cross the blood-brain barrier either directly, or indirectly, through infected endothelial cells, macrophages, or the axons of olfactory or peripheral neurons [10]. WNF is characterised by a sudden onset of symptoms that may include headache, malaise, fever, myalgia, vomiting, papular rash, fatigue, and eye pain [11]. Symptom severity ranges from a mild self-limiting illness from which patients recover within one week to protracted fatigue and malaise that can last for months. The cornerstone of diagnosis remains positive serology for acute infection that usually converts after the first week of disease initiation [12]. Viremia, like in the case of other flaviviruses, is of low levels and of short duration. Treatment is symptomatic; while effective vaccines have been licensed for the prophylaxis of equids, no FDA-approved vaccine exists for human use yet [13].

2. Transmission Vectors, Life Cycle and Animal Hosts of WNV

WNV is maintained in nature in an enzootic transmission cycle between avian hosts and ornithophilic mosquito vectors. Besides the main hosts/reservoirs which will develop WNV disease, outbreaks may develop in horses and humans, with systemic symptomatology [14]. They become infected accidentally and represent dead-end hosts (Scheme 1). The virus is transmitted almost exclusively by mosquitoes, mostly species of Culex, along with the Japanese encephalitis and Murray Valley encephalitis viruses [15]. Although of indeterminate significance, WNV has been detected in ticks (Hyalomma marginatum marginatum nymph) [16]. In Europe, the ornithophilic mosquito species Culex pipiens (biotype) pipiens and Culex pipiens (biotype) molestus are the main vectors of WNV south of the Alps, with Culex torrentium being the dominant species in northern Europe [17].
Besides Culicidae, experimental data additionally confirmed the capacity of Aedes and other mosquitoes to transmit WNV [18]; in fact, efficient transmission has been experimentally demonstrated with most of the evaluated mosquito species. Being an efficient vector requires regular feeding on competent hosts. Aedes albopictus, an invasive tiger mosquito with behavioural characteristics which render it a public health threat in terms of potential contribution to the manifestation of emerging infectious disease outbreaks, is proven to be a competent vector in laboratory settings. In praxis, it is considered to be of little importance for transmission as these species mainly bite mammals and are thus unlikely to acquire the infection from birds [19,20]. In contrast, the Culex pipiens (biotype) pipiens prefers feeding on birds and plays an important role in the enzootic transmission cycle of WNV.

3. WNV Disease: An Emerging or Re-Emerging Infectious Disease?

According to serological surveys, WNV has circulated in Europe since the 1950s [21], and the first recognized human outbreak was recorded in 1962–1963 in Camargue, Southern France [22]. However, up until 1996, the cases that were reported were sporadic. In the past two decades, outbreaks have been recorded practically annually, both in animals as well as humans (ECDC, Historical data by year—West Nile virus seasonal surveillance). Several epidemiological studies have tried to address the causes for its evolution to an emerging infectious disease and have focused both on inherent viral factors as well as extrinsic (environmental, vector-associated and/or human) ones.
The sustainability of WNF outbreaks in South-eastern Europe since 2010 presumes the overwintering of the virus in the region. In support of this theory, the same WNV strain that was identified during the 2010 outbreak in Greece was isolated from sentinel chickens in 2011 from neighbouring regions, indicating the ability of the virus to overwinter in this region [23]. Additionally, viral seropositivity of non-migratory bird species would suggest that these may provide a reservoir for infection of mosquitoes and further transmission of the virus or other avian species which thus do not need to migrate to Africa to become infected [24].
The major factor currently favouring viral overwintering in contrast to previous decades appears to be the rise of the median winter temperatures to levels permissive for vector survival [25]. The theory that the introduction of new vectors, such as the Aedes tiger mosquitoes which are adapted to humanized urbanized environments, would have contributed significantly is not supported by the current evidence.

4. Climate Factor Deviations and Mosquito-Borne Disease Expansion

Climate change is considered to be a major contributing factor to the global expansion of mosquito-borne diseases, previously restricted to tropical and subtropical areas [26]. Outbreaks of Chikungunya and West Nile virus disease, and autochthonous cases of Dengue fever and infections caused by Zika virus, have been reported in several countries of South and South-eastern Europe in the past 20 years [27,28,29,30]. The detection of cases not associated with travel to endemic regions and the spread of these pathogens to geographical areas previously unfamiliar with them has been associated with factors directly connected to, or indirectly attributable to, climate change. Lower mean annual winter and higher spring and summer temperatures have all been associated with the increased risk for epidemic outbreaks. However, evidence is not always conclusive [31,32,33,34]. Vectors, in this case mosquitoes, replicate, and in general function above a threshold temperature of 10 °C [35]. With elevation of the temperature within tolerable limits, their replication cycle shortens and feeding has to increase, and this translates into increasing biting frequency. Taking into account that under moderately elevated temperatures virogenesis is also augmented, it can reasonably be assumed that global warming leads to increased pathogen transmission to the susceptible hosts [36,37]. However, historical examples of three prominent mosquito-borne diseases (malaria, yellow fever, and dengue) have challenged the significance of temperature compared to other environmental or human—inflicted modifications of the regional ecology [38].
Besides the greenhouse effect, the extreme weather phenomena recorded in association with global climate change influence ecosystems through increased precipitation, leading to shifts in relative humidity; also dependent on mean temperature and ground moisture. Once more, humidity appears to have conflicting effects on the spread of mosquito-borne diseases [39]. The increased relative humidity was associated with and increased survival rate of Aedes albopictus, but not Culex sp. in separate reports [31,40]. However, observed biting rates consistently relate to drier conditions [41,42]. Soil moisture is interrelated with regional vegetation cover and exerts a mixed effect on the transmission of WNV dependent on temperature variations [43]. Table 1 summarizes climate factors which have been implicated in the development of outbreaks of mosquito-borne emerging infectious diseases in Europe.
In 2010, a big WNV infection outbreak was recorded in Europe, particularly in the South-eastern part, both in humans as well as in equids. The summer of 2010 was characterised by exceptionally hot temperatures, with temperature elevations of more than 5 °C above the usual ones. It is presumed that the heat wave may indeed have contributed to the development of the epidemic [57]. Whether or not this association is always valid has not been addressed yet. Figure 1 correlates the average temperature, precipitation, relative humidity, and soil moisture anomalies of January, April, and July, representing winter, spring, and early summer, respectively, of each year in Greece from 2010 to 2023, compared with the average values during the reference period 1991–2020, to investigate potential associations with the intensity of each year’s epidemic. The two major epidemics of 2010 and 2018 in Greece since 2010 are highlighted by the oval shape and addressed separately.

5. Contribution of the Newly Translocated Arthropod Vectors to WNV Outbreaks in Europe

The migration, in fact, the transportation in tyres or with transport media, and the settling of the invasive tiger mosquitos (Aedes sp.) in the European continent sounded the alarm for public health authorities [58]. The two major factors ecologically favouring their local installation are considered to be climate warming and the increasing urbanization [59]. The establishment of these tropical mosquitos is considered, per se, to increase the risk for emerging infectious disease outbreaks due to their specific properties which clearly distinguish them from the currently circulating Culex sp. First of all, they are able to infestate urbanized areas, in which they and the eggs that they lay can survive considerably long. In terms of feeding habits, they preferentially bite humans and they will bite throughout the daytime, but do so mostly at dawn and dusk. Their most important characteristic is that they represent very well-adapted vectors to all the mosquito-borne viruses implicated in, and predicted to, further cause emerging infectious disease outbreaks (Chikungunya, West Nile, Dengue, Zika) [49]. Six invasive Aedes mosquito species have migrated to Europe since the 1970s: Aedes aegypti, Aedes albopictus, Aedes japonicus, Aedes koreicus, Aedes atropalpus, and Aedes triseriatus. However, the first pan-European surveillance effort organized in 2020 recorded the presence of two of them, Aedes albopictus and Aedes japonicus along with the native Culicidae [60]. Aedes aegypti, although present in the continent since the early 20th century, disappeared in the 60s, only to become reimported in 2008 in the area of Caucasus and the Black Sea [61]. For not fully apprehended reasons, however, despite its spreading west along the Black Sea coast, it is not yet established anywhere in the region in contrast to North America, probably due to other conditions, not presently fulfilled in Europe or even the properties and characteristics of the particular Mediterranean ecotype population of Aedes aegypti, clearly different from the American and Asian populations [62].
Aedes albopictus, on the other hand, originating from Southeast Asia, appeared in Albania in 1979, but finally settled in the Mediterranean Basin in 1990, when it was isolated again in a playground in Italy [50]. In contrast to Aedes aegypti, Aedes albopictus has demonstrated a remarkably widespread global distribution, now listed as one of the top 100 invasive species by the Invasive Species Specialist Group [51]. This differential adaptation is partly attributed to its increased tolerance of lower temperatures, that is, stronger adaptation to temperature instabilities [52], enabling it, theoretically regionally, to prevail and attenuate the installation of other invasive mosquitos. In comparison to its counterpart, Aedes aegypti, this species feeds on a wide range of hosts, thus theoretically presenting a serious public health threat as a bridge vector of zoonotic pathogens to humans [63].
Despite their potency to effectively transmit Flaviviridae and Togaviridae, in active mosquito surveillance systems which were implemented after outbreaks of West Nile fever mainly in South-eastern Europe, e.g., Greece, WNV was only detected in Culex pipiens complex mosquito pools in several instances [64,65]. Sixteen studies investigated the probability of different vectors’ WNV carriage in association with factors/locations affecting their breeding [66]. Culex pipiens complex was repeatedly identified as the key WNV vector, clearly indicating that the biological selection of the vector that will overtake the transmission of the pathogen is dependent on a wide, potentially circumstantial range of factors and has surely not been fully clarified yet.

6. The Impact of Socioeconomic Factors on Vector-Borne Diseases

Anthropogenic factors such as urbanization, human activities associated with the spreading of arthropod vectors outside their historical habitats, or other conditions with socioeconomic impact have, in several studies, been associated both with an amplified WNV presence in vectors and with increased incidence of WNV-associated disease [67]. Densely populated urbanized areas are associated with older infrastructure, impaired water drainage systems, and insufficient sanitation [68]. Lower-income communities are less aware of the public health risks that are inextricably linked to the creation of vector hotspots and do not demand, as firmly, pest control interventions [69]. Results from a study performed in Tennessee indicated, among others, that indeed vector abundance was higher in lower-income urban areas compared to higher-income ones [70].
During periods of austerity, governments may have to cut back on public health preservation efforts, such as spending on flood prevention measures, sanitation, and wastewater management, but also public education programs and health promotion [25]. The dysfunction of healthcare systems may additionally contribute to the aggravation of emerging infectious disease outbreaks. The beginning of the 21st-century era was characterised by a global financial recession. During Greece’s recent economic turmoil, from its initial manifestation in July 2010 until December 2011, that is, within a period of 18 months only, three infectious disease outbreaks took place. Aside from the increased mortality of the influenza epidemic that was recorded during the same period, the outbreaks included: an outbreak of West Nile virus infection in the summer and early autumn of 2010, with 197 reported patients with neuroinvasive disease and 35 total deaths, in the geographical area of Northern Greece; an outbreak of malaria in southern Greece during the summer of 2011 with 63 reported cases, of which 40 were considered autochthonous (non-imported); and an epidemic wave of new Human Immunodeficiency Virus cases with a 57.2% increase in newly diagnosed cases and a 1506.7% increase of newly diagnosed cases in injection drug users [71]. Environmental factors indisputably represent the leading cause of these epidemiological crises. However, the previously presented data can only support the theory that the austerity measures imposed upon the health sector, social services, and healthcare politics in Greece appear to have had a significant impact on public health.

7. West Nile Virus: An Endemic Pathogen in Greece

Before 2008, WNV outbreaks in Europe involved few cases and faded out very abruptly with minimal cases in the consecutive couple of years under very stringent surveillance [72].
Up until 2010, no human cases had been described in Greece. Seropositivity in studies was 1% among farmers [73]; the prevalence was significantly higher among animals, however, reaching 24% in birds [74]. Retrospective analysis of serum samples from inhabitants of Imathia, an area in Central Macedonia, which had a leading role in the majority of the outbreaks recorded in Greece from 2010 onwards, showed similarly a positivity rate of 1.02% [75].
In the summer of 2010, Greece experienced its first outbreak of West Nile virus infections, recording 262 cases in total and 35 deaths [76]. Since 2010, Greece has experienced annual outbreaks throughout, with variable intensity, with only a 2-year interval without any recorded cases (2015–2016) [77]. Seropositivity in the corresponding area of Greece (prefecture of Imathia and Pella) rose within weeks of the first outbreak from roughly 1.0 to 5.8% [78]. In these 14 years, from 2010 until now, a total of 1603 verified cases of West Nile fever have been reported in Greece in a total of 32/51 prefectures, progressively expanding (Figure 2). It needs to be stressed that the number of verified recorded cases each year is only a small proportion of the actual ones and refers to the patients who develop persistent symptomatology or present with a more severe clinical condition qualifying for further investigation. Moreover, the mapping of the geographical distribution of the cases may not completely coincide with the actual site of infection, due to travelling and people translocation. Specific areas, mainly in the northern and central mainland, are considered WNV “hot spots” as they consistently record confirmed WNF cases during the annual epidemics [79].
Integrated surveillance protocols, implemented in Greece since the first outbreak, included obligatory notification of verified human cases and active sentinel surveillance of vectors from mosquito traps and equids, indicating the steady presence of the virus throughout, irrespective of whether human cases were recorded during a particular year (2015–2016 were theoretically free of recorded, at least, WNV cases) [80].
The majority of the outbreaks recorded in Europe in the past two decades (since 2008), including the annual outbreaks in Greece, were attributed to the neurovirulent strain belonging to lineage 2, which was imported to Europe from Africa and has since then become established in the area [81]. A recently published epidemiological report from Greece’s National Public Health Organization (EODY) and the National Reference Laboratories, collecting and molecularly characterising viral strains detected in patients, blood donors mosquitoes, horses, and birds since 2010, reported that all but one WNV sequence clustered into the Central European subclade of WNV lineage 2 [79]. A viral strain belonging to the Eastern European/Russian subclade of WNV lineage 2 was detected in a patient from north-eastern Greece in 2018, indicating the introduction of a new virus in the area [82]. Clearly, the formerly considered to be an emerging infectious disease pathogen has become an endemic pathogen, well established in the region.

8. Comparison of Climatic Anomalies, Hydrological Variables, and Annual WNF Outbreaks in Greece

Annual data extracted from the Copernicus Climate Change Service/ECMWF concerning climatic and hydrological parameters were juxtaposed to the annual WNF epidemics from the Greek National Centre for Disease Control Registry, [National Public Health Organization-EODY, annual WNV surveillance reports (2010–2023)]. January, April, and July were chosen to represent winter, spring and summer, respectively. Temperature and precipitation anomalies, as well as relative humidity and soil moisture deviations, were compared to the intensity of the annual WNF epidemic waves (Figure 2). Interestingly, the two more pronounced WNF outbreaks of 2010 and 2018, of 262 and 316 WNF cases, respectively, were associated with a warmer winter; a warmer, drier spring; and a more humid, not necessarily warmer, summer (oval shapes). These results suggest that indeed global warming may facilitate vector hibernation, and warm, drier springs may accelerate earlier WNV transmission, resulting in a higher circulation during the following months, while increased humidity during the summer contributes to the peaking of mosquito-borne diseases, probably by accelerating the vectors’ reproduction [83,84].

9. Conclusions

WNV has been established in the area of South, South-eastern and, lately, Western and Central Europe, and is spreading towards its northern part with the aid of climate change, which in turn facilitates its potential to survive and spread in previously inhospitable regions [85]. Outbreaks of locally acquired infections are recorded annually, rendering WNV the leading cause of arboviral disease, not only in the US, but also in Europe [86,87]. According to the report of the European Food Safety Authority and the European Centre for Disease Prevention and Control concerning the results of zoonoses’ monitoring and surveillance activities, WNV together with Listeriosis is the most severe zoonotic disease, with the most hospitalisations and the highest morbidity [88].
Greece ranks among the countries with the highest annual notification rates with significant fluctuations, or rather, with an irregular wavy pattern in the intensity of its outbreaks. Annual reported symptomatic cases in the years from 2010 to 2022 varied from 0 to 311 with a notification rate for West Nile cases with neuroinvasive disease ranging from 0 to 2.2 per 100,000 population. The associated mortality rate ranged from 9% to 40%. Initiation of each year’s epidemic fluctuated and was recorded from as early as May 31st with the detection of the first annual case up to as late as August 5th. Years with a higher epidemiological burden were usually characterised by an early start of the epidemic [79].
Predicting the severity of each year’s epidemic seems unrealistic as a variety of factors exert their effect and interrelate in a highly complex manner. An intense previous season justifies public health authorities’ alertness. Recording of WNF cases in a geographical area during the summer to early autumn of a specific year carries a risk of recurrence of WNV infections in the same region of up to 50% for the next month of the season and 20% for the subsequent year [89].
Climate factors favouring potential outbreaks are more versatile and affect geographical regions relative to their native climatic conditions. In an epidemiological study from Spain, the combination of high precipitation rates, soil moisture, and a warmer spring provided more favourable environmental conditions for mosquitoes to breed and transmit WNV [90], in agreement with our analysis.
As the virus has gained endemicity in the region and has already been steadily circulating for more than a decade, perhaps the most reliable tool to predict the next epidemic at this point is to monitor mosquito-borne viral activity prior to the initiation and throughout each year’s candidate season. Greece has one of the most organized WNV surveillance programs [91]. Increases in the mosquito viral positivity rates aid public health authorities to promptly adopt emergency measures to halt the potential development of an outbreak, such as the implementation of vector control measures and the use of biocides.
WNV and other flaviviruses have expanded their distribution significantly and are expected to increasingly burden public health systems in the future. It therefore is of particular significance to develop reliable outbreak prediction tools adjusted to each particular pathogen’s ecology that will be implemented in order to limit the spread of the virus and lessen the impact of the forthcoming epidemic.

Author Contributions

Conceptualization, D.K. and A.P.; Methodology D.K. and K.C.; Software K.C.; Analysis D.K., K.C., A.P.; Preparation of the manuscript D.K., K.C., A.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Rossi, S.L.; Ross, T.M.; Evans, J.D. West Nile Virus. Clin. Lab. Med. 2010, 30, 47–65. [Google Scholar] [CrossRef] [PubMed]
  2. Brinton, M.A. The molecular biology of West Nile Virus: A new invader of the western hemisphere. Annu. Rev. Microbiol. 2002, 56, 371–402. [Google Scholar] [CrossRef] [PubMed]
  3. Saiz, J.-C.; Martín-Acebes, M.A.; Blázquez, A.B.; Escribano-Romero, E.; Poderoso, T.; de Oya, N.J. Pathogenicity and virulence of West Nile virus revisited eight decades after its first isolation. Virulence 2021, 12, 1145–1173. [Google Scholar] [CrossRef] [PubMed]
  4. Chancey, C.; Grinev, A.; Volkova, E.; Rios, M. The global ecology and epidemiology of West Nile virus. Biomed. Res. Int. 2015, 2015, 376230. [Google Scholar] [CrossRef] [PubMed]
  5. Hernández-Triana, L.M.; Jeffries, C.L.; Mansfield, K.L.; Carnell, G.; Fooks, A.R.; Johnson, N. Emergence of west nile virus lineage 2 in europe: A review on the introduction and spread of a mosquito-borne disease. Front. Public Health 2014, 2, 271. [Google Scholar] [CrossRef]
  6. McMullen, A.R.; Albayrak, H.; May, F.J.; Davis, C.T.; Beasley, D.W.C.; Barrett, A.D.T. Molecular evolution of lineage 2 West Nile virus. J. Gen. Virol. 2013, 94, 318–325. [Google Scholar] [CrossRef]
  7. Campbell, G.L.; Marfin, A.A.; Lanciotti, R.S.; Gubler, D.J. West Nile virus. Lancet Infect. Dis. 2002, 9, 519–529. [Google Scholar] [CrossRef]
  8. Petersen, L.R.; Brault, A.C.; Nasci, R.S. West Nile virus: Review of the literature. JAMA 2013, 310, 308–315. [Google Scholar] [CrossRef]
  9. Pingen, M.; Schmid, M.A.; Harris, E.; McKimmie, C.S. Mosquito Biting Modulates Skin Response to Virus Infection. Trends Parasitol. 2017, 33, 645–657. [Google Scholar] [CrossRef]
  10. Cho, H.; Diamond, M.S. Immune responses to West Nile virus infection in the central nervous system. Viruses 2012, 4, 3812–3830. [Google Scholar] [CrossRef]
  11. Zou, S.; Foster, G.A.; Dodd, R.Y.; Petersen, L.R.; Stramer, S.L. West Nile fever characteristics among viremic persons identified through blood donor screening. J. Infect. Dis. 2010, 202, 1354–1361. [Google Scholar] [CrossRef] [PubMed]
  12. Hayes, E.B.; Sejvar, J.J.; Zaki, S.R.; Lanciotti, R.S.; Bode, A.V.; Campbell, G.L. Virology, Pathology, and Clinical Manifestations of West Nile Virus Disease. Emerg. Infect. Dis. 2005, 11, 1174–1179. [Google Scholar] [CrossRef] [PubMed]
  13. Suthar, M.S.; Diamond, M.S.; Gale, M., Jr. West Nile virus infection and immunity. Nat. Rev. Microbiol. 2013, 11, 115–128. [Google Scholar] [CrossRef] [PubMed]
  14. Martín-Acebes, M.A.; Saiz, J.-C. West Nile virus: A re-emerging pathogen revisited. World J. Virol. 2012, 12, 51–70. [Google Scholar] [CrossRef] [PubMed]
  15. Kain, M.P.; Skinner, E.B.; Athni, T.S.; Ramirez, A.L.; Mordecai, E.A.; van den Hurk, A.F. Not all mosquitoes are created equal: A synthesis of vector competence experiments reinforces virus associations of Australian mosquitoes. PLoS Negl. Trop. Dis. 2022, 16, e0010768. [Google Scholar] [CrossRef] [PubMed]
  16. Vasić, A.; Oșlobanu, L.E.; Marinov, M.; Crivei, L.A.; Rățoi, I.A.; Aniță, A.; Aniță, D.; Doroșencu, A.; Alexe, V.; Răileanu, S.; et al. Evidence of West Nile Virus (WNV) Circulation in Wild Birds and WNV RNA Negativity in Mosquitoes of the Danube Delta Biosphere Reserve, Romania, 2016. Trop Med. Infect. Dis. 2019, 4, 116. [Google Scholar] [CrossRef]
  17. Jansen, S.; Heitmann, A.; Lühken, R.; Leggewie, M.; Helms, M.; Badusche, M.; Rossini, G.; Schmidt-Chanasit, J.; Tannich, E. Culex torrentium: A Potent Vector for the Transmission of West Nile Virus in Central Europe. Viruses 2019, 11, 492. [Google Scholar] [CrossRef]
  18. Ciota, A.T. West Nile virus and its vectors. Curr. Opin. Insect. Sci. 2017, 22, 28–36. [Google Scholar] [CrossRef]
  19. Kilpatrick, A.M.; Kramer, L.D.; Jones, M.J.; Marra, P.P.; Daszak, P. West Nile virus epidemics in North America are driven by shifts in 810 mosquito feeding behavior. PLoS Biol. 2006, 4, e82. [Google Scholar] [CrossRef]
  20. Vogels, C.B.; Göertz, G.P.; Pijlman, G.P.; Koenraadt, C.J. Vector competence of European mosquitoes for West Nile virus. Emerg. Microbes Infect. 2017, 6, e96. [Google Scholar] [CrossRef]
  21. Bardos, V.; Adamcova, J.; Dedei, S.; Gjini, N.; Rosicky, B.; Simkova, A. Neutralizing antibodies against some neurotropic viruses determined in human sera in Albania. J. Hyg. Epidemiol. Microbiol. Immunol. 1959, 3, 277–282. [Google Scholar]
  22. Joubert, L.; Oudar, J.; Hannoun, C.; Beytout, D.; Corniou, B.; Guillon, J.C.; Panthier, R. Epidemiology of the West Nile virus: Study of a focus in Camargue. IV. Meningo-encephalomyelitis of the horse. Ann. Inst. Pasteur. 1970, 118, 239–247. [Google Scholar]
  23. Chaskopoulou, A.; Dovas, C.I.; Chaintoutis, S.C.; Bouzalas, I.; Ara, G.; Papanastassopoulou, M. Evidence of enzootic circulation of West Nile virus (Nea Santa-Greece-2010, lineage 2), Greece, May to July 2011. Eur. Surveill. 2011, 16, 19933. [Google Scholar] [CrossRef]
  24. Malkinson, M.; Banet, C. The role of birds in the ecology of West Nile virus in Europe and Africa. Curr. Top Microbiol. Immunol. 2002, 267, 309–322. [Google Scholar] [PubMed]
  25. Watts, M.J.; Monteys, V.S.I.; Mortyn, P.G.; Kotsila, P. The rise of West Nile Virus in Southern and Southeastern Europe: A spatial-temporal analysis investigating the combined effects of climate, land use and economic changes. One Health 2021, 13, 100315. [Google Scholar] [CrossRef] [PubMed]
  26. Beermann, S.; Dobler, G.; Faber, M.; Frank, C.; Habedank, B.; Hagedorn, P.; Kampen, H.; Kuhn, C.; Nygren, T.; Schmidt-Chanasit, J.; et al. Impact of climate change on vector- and rodent-borne infectious diseases. J. Health Monit. 2023, 8, 33–61. [Google Scholar]
  27. Rezza, G.; Nicoletti, L.; Angelini, R.; Romi, R.; Finarelli, A.C.; Panning, M. Infection with chikungunya virus in Italy: An outbreak in a temperate region. Lancet 2007, 370, 1840–1846. [Google Scholar] [CrossRef] [PubMed]
  28. Emmanouil, M.; Evangelidou, M.; Papa, A.; Mentis, A. Importation of dengue, Zika and chikungunya infections in Europe: The current situation in Greece. New Microbes New Infect. 2020, 35, 100663. [Google Scholar] [CrossRef]
  29. Cochet, A.; Calba, C.; Jourdain, F.; Grard, G.; Durand, G.A.; Guinard, A.; Investigation Team; Noël, H.; Paty, M.C.; Franke, F. Autochthonous dengue in mainland France, 2022: Geographical extension and incidence increase. Eur. Surveill. 2022, 27, 2200818. [Google Scholar] [CrossRef]
  30. European Center for Disease Control (ECDC), Stockholm, Sweden. Zika Virus Disease in Var Department, France. ECDC. 2019. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/RRA-Zika-France-16-Oct-2019-corrected.pdf (accessed on 16 October 2022).
  31. Sauer, F.G.; Timmermann, E.; Lange, U.; Lühken, R.; Kiel, E. Effects of Hibernation Site, Temperature, and Humidity on the Abundance and Survival of Overwintering Culex pipiens pipiens and Anopheles messeae (Diptera: Culicidae). J. Med. Entomol. 2022, 59, 2013–2021. [Google Scholar] [CrossRef]
  32. Reisen, W.K.; Wheeler, S.S. Overwintering of West Nile Virus in the United States Review. J. Med. Entomol. 2019, 56, 1498–1507. [Google Scholar] [CrossRef] [PubMed]
  33. Marini, G.; Manica, M.; Delucchi, L.; Pugliese, A.; Rosà, R. Spring temperature shapes West Nile virus transmission in Europe. Acta Trop. 2021, 215, 105796. [Google Scholar] [CrossRef] [PubMed]
  34. Marcantonio, M.; Rizzoli, A.; Metz, M.; Rosà, R.; Marini, G.; Chadwick, E.; Neteler, M. Identifying the Environmental Conditions Favouring West Nile Virus Outbreaks in Europe. PLoS ONE 2015, 10, e0121158. [Google Scholar] [CrossRef] [PubMed]
  35. Ciota, A.T.; Keyel, A.C. The Role of Temperature in Transmission of Zoonotic Arboviruses. Viruses 2019, 11, 1013. [Google Scholar] [CrossRef]
  36. Farooq, Z.; Sjödin, H.; Semenza, J.C.; Tozan, Y.; Sewe, M.O.; Wallin, J.; Rocklöva, J. European projections of West Nile virus transmission under climate change scenarios. One Health 2023, 16, 100509. [Google Scholar] [CrossRef]
  37. Liu, Z.; Zhang, Z.; Lai, Z.; Zhou, T.; Jia, Z.; Gu, J.; Wu, K.; Chen, X.G. Temperature Increase Enhances Aedes albopictus Competence to Transmit Dengue Virus. Front. Microbiol. 2017, 8, 2337. [Google Scholar] [CrossRef]
  38. Reiter, P. Climate change and mosquito-borne disease. Rev. Environ. Health Perspect. 2001, 109, 141–161. [Google Scholar]
  39. Brown, J.J.; Pascual, M.; Wimberly, M.C.; Johnson, L.R.; Murdock, C.C. Humidity—The overlooked variable in the thermal biology of mosquito-borne disease. Ecol. Lett. 2023, 26, 1029–1049. [Google Scholar] [CrossRef]
  40. Cai, X.; Zhao, J.; Deng, H.; Xiao, J.; Liu, T.; Zeng, W.; Li, X.; Hu, J.; Huang, C.; Zhu, G.; et al. Effects of temperature, relative humidity, and illumination on the entomological parameters of Aedes albopictus: An experimental study. Int. J. Biometeorol. 2023, 67, 687–694. [Google Scholar] [CrossRef]
  41. Lindsay, S.W.; Wilkins, H.A.; Zieler, H.A.; Daly, R.J.; Petrarca, V.; Byass, P. Ability of Anopheles gambiae mosquitoes to transmit malaria during the dry and wet seasons in an area of irrigated rice cultivation in The Gambia. J. Trop. Med. Hyg. 1991, 94, 313–324. [Google Scholar]
  42. Chow, W.K.; Beebe, N.W.; Ambrose, L.; Pickering, P.; Cooper, R.D. Seasonal assessment on the effects of time of night, temperature and humidity on the biting profile of Anopheles farauti in north Queensland, Australia using a population naive to malaria vector control pressures. Malar. J. 2023, 22, 85. [Google Scholar] [CrossRef] [PubMed]
  43. Keyel, A.C.; Timm, O.E.; Backenson, P.B.; Prussing, C.; Quinones, S.; McDonough, K.A.; Vuille, M.; Conn, J.E.; Armstrong, P.M.; Andreadis, T.G.; et al. Seasonal temperatures and hydrological conditions improve the prediction of West Nile virus infection rates in Culex mosquitoes and human case counts in New York and Connecticut. PLoS ONE 2019, 14, e0217854. [Google Scholar] [CrossRef] [PubMed]
  44. Gorris, M.E.; Randerson, J.T.; Coffield, S.R.; Treseder, K.K.; Zender, C.S.; Xu, C.; Manore, C.A. Assessing the Influence of Climate on the Spatial Pattern of West Nile Virus Incidence in the United States. Environ. Health Perspect. 2023, 131, 047016. [Google Scholar] [CrossRef]
  45. Tran, A.; Sudre, S.; Paz, S.; Rossi, M.; Desbrosse, A.; Chevalier, V.; Semenza, J.C. Environmental predictors of West Nile fever risk in Europe. Int. J. Health Geogr. 2014, 13, 26. [Google Scholar] [CrossRef] [PubMed]
  46. Cotar, A.I.; Falcuta, E.; Prioteasa, L.F.; Dinu, S.; Ceianu, C.S.; Paz, S. Transmission Dynamics of the West Nile Virus in Mosquito Vector Populations under the Influence of Weather Factors in the Danube Delta, Romania. EcoHealth 2016, 13, 796–807. [Google Scholar] [CrossRef]
  47. Paz, S.; Albersheim, I. Influence of warming tendency on Culex Pipiens population abundance and on the probability of West Nile Fever outbreaks (Israeli Case Study: 2001–2005). EcoHealth 2008, 5, 40–48. [Google Scholar] [CrossRef]
  48. Korytár, L.; Peňazziová, K.; Pistl, J.; Tichá, E.; Čabanová, V.; Csank, T. Retrospective review and current knowledge on the occurrence of West Nile virus in mosquito vectors, reservoirs and hosts in Slovakia (Central Europe). Acta Virol. 2020, 64, 187–200. [Google Scholar] [CrossRef] [PubMed]
  49. Benelli, G.; Wilke, A.B.B.; Beier, J.C. Aedes albopictus (Asian tiger mosquito). Trends Parasitol. 2020, 36, 942–943. [Google Scholar] [CrossRef]
  50. Oliveira, S.; Rocha, J.; Sousa, C.A.; Capinha, C. Wide and increasing suitability for Aedes albopictus in Europe is congruent across distribution models. Sci. Rep. 2021, 11, 9916. [Google Scholar] [CrossRef]
  51. European Center for Disease Control (ECDC), Stockholm, Sweden. Aedes Albopictus—Factsheet for Experts, 20 December 2016. Available online: https://www.ecdc.europa.eu/en/disease-vectors/facts/mosquito-factsheets/aedes-albopictus (accessed on 20 August 2023).
  52. Laporta, G.Z.; Potter, A.M.; Oliveira, J.F.A.; Bourke, B.P.; Pecor, D.B.; Linton, Y.-M. Global Distribution of Aedes aegypti and Aedes albopictus in a Climate Change Scenario of Regional Rivalry. Insects 2023, 14, 49. [Google Scholar] [CrossRef]
  53. Montecino-Latorre, D.; Barker, C.M. Overwintering of West Nile virus in a bird community with a communal crow roost. Sci. Rep. 2018, 8, 6088. [Google Scholar] [CrossRef] [PubMed]
  54. Kampen, H.; Tews, B.A.; Werner, D. First Evidence of West Nile Virus Overwintering in Mosquitoes in Germany. Viruses 2021, 13, 2463. [Google Scholar] [CrossRef] [PubMed]
  55. Kjellstrom, T.; Friel, S.; Dixon, J.; Corvalan, C.; Rehfuess, E.; Campbell-Lendrum, D.; Gore, F.; Bartram, J. Urban environmental health hazards and health equity. J. Urban Health 2007, 84, 86–97. [Google Scholar] [CrossRef]
  56. Kondilis, E.; Giannakopoulos, S.; Gavana, M.; Ierodiakonou, I.; Waitzkin, H.; Benos, A. Economic crisis, restrictive policies, and the population’s health and health care: The Greek case. Am. J. Public Health 2013, 103, 973–979. [Google Scholar] [CrossRef] [PubMed]
  57. Paz, S.; Malkinson, D.; Green, M.S.; Tsioni, G.; Papa, A.; Danis, K.; Sirbu, A.; Ceianu, C.; Katalin, K.; Ferenczi, E.; et al. Permissive summer temperatures of the 2010 European West Nile fever upsurge. PLoS ONE 2013, 8, e56398. [Google Scholar] [CrossRef]
  58. Gratz, N.G. Critical review of the vector status of Aedes albopictus. Med. Vet. Entomol. 2004, 18, 215–227. [Google Scholar] [CrossRef]
  59. Giunti, G.; Becker, N.; Benelli, G. Invasive mosquito vectors in Europe: From bioecology to surveillance and management. Acta Trop. 2023, 239, 106832. [Google Scholar] [CrossRef]
  60. Miranda, M.M.; Barceló, C.; Arnoldi, D.; Augsten, X.; Bakran-Lebl, K.; Balatsos, G.; Bengoa, M.; Bindler, P.; Boršová, K.; Bourquia, M.; et al. Consortium AIM-COST/AIM-Surv AIMSurv: First pan-European harmonized surveillance of Aedes invasive mosquito species of relevance for human vector-borne diseases. GigaByte 2022, 2022, gigabyte57. [Google Scholar]
  61. Wint, W.; Jones, P.; Kraemer, M.; Alexander, N.; Schaffnerd, F. Past, present and future distribution of the yellow fever mosquito Aedes aegypti: The European paradox. Sci. Total Environ. 2022, 847, 157566. [Google Scholar] [CrossRef]
  62. Trájer, A.J. Aedes aegypti in the Mediterranean container ports at the time of climate change: A time bomb on the mosquito vector map of Europe. Heliyon 2021, 7, e07981. [Google Scholar] [CrossRef]
  63. Eritja, R.; Escosa, R.; Lucientes, J.; Marques, E.; Roiz, D.; Ruiz, S. Worldwide invasion of vector mosquitoes: Present European distribution and challenges in Spain. Biol Invasions 2005, 7, 87–97. [Google Scholar] [CrossRef]
  64. Mavridis, K.; Fotakis, E.A.; Kioulos, I.; Mpellou, S.; Konstantas, S.; Varela, E.; Gewehr, S.; Diamantopoulos, V.; Vontas, J. Detection of West Nile virus—Lineage 2 in Culex pipiens mosquitoes, associated with disease outbreak in Greece, 2017. Acta Trop. 2018, 182, 64–68. [Google Scholar] [CrossRef] [PubMed]
  65. Patsoula, E.; Vakali, A.; Balatsos, G.; Pervanidou, D.; Beleri, S.; Tegos, N.; Baka, A.; Spanakos, G.; Georgakopoulou, T.; Tserkezou, P.; et al. West Nile virus circulation in mosquitoes in Greece (2010–2013). Biomed. Res. Int. 2016, 2016, 2450682. [Google Scholar] [CrossRef] [PubMed]
  66. Giesen, C.; Herrador, Z.; Fernandez-Martinez, B.; Figuerola, J.; Gangoso, L.; Vazquez, A.; Gómez-Barroso, D. A systematic review of environmental factors related to WNV circulation in European and Mediterranean countries. One Health 2023, 16, 100478. [Google Scholar] [CrossRef] [PubMed]
  67. Cuthbert, R.N.; Darriet, F.; Chabrerie, O.; Lenoir, J.; Courchamp, F.; Claeys, C.; Robert, V.; Jourdain, F.; Ulmer, R.; Diagne, C.; et al. Invasive hematophagous arthropods and associated diseases in a changing world. Parasit. Vectors 2023, 16, 291. [Google Scholar] [CrossRef]
  68. Harrigan, R.J.; Thomassen, H.A.; Buermann, W.; Cummings, R.F.; Kahn, M.E.; Smith, T.B. Economic conditions predict prevalence of West Nile virus. PLoS ONE 2010, 5, e15437. [Google Scholar] [CrossRef]
  69. Kouamé, R.M.A.; Guglielmo, F.; Abo, K.; Ouattara, A.F.; Chabi, J.; Sedda, L.; Donnelly, M.J.; Edi, C. Education and So-cio-economic status are key factors influencing use of insecticides and malaria knowledge in rural farmers in Southern Côte d’Ivoire. BMC Public Health 2022, 22, 2443. [Google Scholar] [CrossRef]
  70. Savage, H.M.; Anderson, M.; Gordon, E.; McMillen, L.; Colton, L.; Delorey, M.; Sutherland, G.; Aspen, S.; Charnetzky, D.; Burkhalter, K. Host-seeking heights, host-seeking activity patterns, and West Nile virus infection rates for members of the Culex pipiens complex at different habitat types within the hybrid zone, Shelby County, TN, 2002 (Diptera: Culicidae). J Med. Entomol. 2008, 45, 276–288. [Google Scholar] [CrossRef]
  71. Bonovas, S.; Nikolopoulos, G. High-burden epidemics in Greece in the era of economic crisis. Early signs of a public health tragedy. J. Prev. Med. Hyg. 2012, 3, 169–171. [Google Scholar]
  72. Hubalek, Z. European Experience with the West Nile Virus Ecology and Epidemiology: Could It Be Relevant for the New World? Viral Immunol. 2000, 13, 415–426. [Google Scholar] [CrossRef]
  73. Antoniadis, A.; Alexiou-Daniel, S.; Malissiovas, N.; Doutsos, J.; Polyzoni, T.; LeDuc, J.W.; Peters, C.J.; Saviolakis, G. Seroepidemiological survey for antibodies to arboviruses in Greece. In Archives of Virology Supplementum; Springer: Vienna, Austria, 1990; Suppl. 1; pp. 277–285. [Google Scholar]
  74. Valiakos, G.; Touloudi, A.; Athanasiou, L.V.; Giannakopoulos, A.; Iacovakis, C.; Birtsas, P.; Spyrou, V.; Dalabiras, Z.; Petrovska, L.; Billinis, C. Serological and molecular investigation into the role of wild birds in the epidemiology of West Nile virus in Greece. Virol. J. 2012, 9, 266. [Google Scholar] [CrossRef] [PubMed]
  75. Papa, A.; Perperidou, P.; Tzouli, A.; Castilletti, C. West Nile virus—Neutralizing antibodies in humans in Greece. Vector Borne Zoonotic Dis. 2010, 10, 655–658. [Google Scholar] [CrossRef] [PubMed]
  76. Danis, K.; Papa, A.; Theocharopoulos, G.; Dougas, G.; Athanasiou, M.; Detsis, M.; Baka, A.; Lytras, T.; Mellou, K.; Bonovas, S.; et al. Outbreak of West Nile virus infection in Greece, 2010. Emerg. Infect. Dis. 2011, 10, 1868–1872. [Google Scholar]
  77. Available online: https://eody.gov.gr/en/epidemiological-statistical-data/annual-epidemiological-data/ (accessed on 23 August 2023).
  78. Ladbury, G.A.F.; Gavana, M.; Danis, K.; Papa, A.; Papamichail, D.; Mourelatos, S.; Gewehr, S.; Theocharopoulos, G.; Bonovas, S.; Benos, A.; et al. Population seroprevalence study after a West Nile virus lineage 2 epidemic, Greece, 2010. PLoS ONE 2013, 8, e80432. [Google Scholar] [CrossRef] [PubMed]
  79. Pervanidou, D.; Kefaloudi, C.N.; Vakali, A.; Tsakalidou, O.; Karatheodorou, M.; Tsioka, K.; Evangelidou, M.; Mellou, K.; Pappa, S.; Stoikou, K.; et al. The 2022 West Nile Virus Season in Greece; A Quite Intense Season. Viruses 2023, 15, 1481. [Google Scholar] [CrossRef] [PubMed]
  80. Gossner, C.M.; Marrama, L.; Carson, M.; Allerberger, F.; Calistri, P.; Dilaveris, D.; Lecollinet, S.; Morgan, D.; Nowotny, N.; Paty, M.-C.; et al. West Nile virus surveillance in Europe: Moving towards an integrated animal-human-vector approach. Eur. Surveill. 2017, 22, 30526. [Google Scholar] [CrossRef]
  81. Bakonyi, T.; Ivanics, E.; Erdelyi, K.; Ursu, K.; Ferenczi, E.; Weissenböck, H.; Nowotny, R. Lineage 1 and 2 strains of encephalitic West Nile virus, central Europe. Emerg. Infect. Dis. 2006, 12, 618–623. [Google Scholar] [CrossRef]
  82. Papa, A.; Papadopoulou, E.; Chatzixanthouliou, C.; Glouftsios, P.; Pappa, S.; Pervanidou, D.; Georgiou, L. Emergence of West Nile Virus Lineage 2 Belonging to the Eastern European Subclade, Greece. Arch. Virol. 2019, 164, 1673–1675. [Google Scholar] [CrossRef]
  83. Magombedze, G.; Ferguson, N.M.; Ghani, A.C. A trade-off between dry season survival longevity and wet season high net reproduction can explain the persistence of anopheles mosquitoes. Parasites Vectors 2018, 11, 576. [Google Scholar] [CrossRef]
  84. Chowdhury, F.R.; Ibrahim, Q.S.U.; Bari, M.S.; Alam, M.M.J.; Dunachie, S.J.; Rodriguez-Morales, A.J.; Patwary, M.I. The associ-ation between temperature, rainfall and humidity with common climate-sensitive infectious diseases in Bangladesh. PLoS ONE 2018, 13, e0199579. [Google Scholar] [CrossRef]
  85. Klingelhöfer, D.; Braun, M.; Kramer, I.M.; Reuss, F.; Müller, R.; Groneberg, D.A.; Brüggmann, D. A virus becomes a global concern: Research activities on West-Nile virus. Emerg. Microbes Infect. 2023, 12, 2256424. [Google Scholar] [CrossRef] [PubMed]
  86. Fagre, A.C.; Lyons, S.; Staples, J.E.; Lindsey, N. West Nile Virus and Other Nationally Notifiable Arboviral Diseases—United States, 2021. MMWR Morb. Mortal Wkly. Rep. 2023, 72, 901–906. [Google Scholar] [CrossRef] [PubMed]
  87. Papa, A. Emerging arboviral human diseases in Southern Europe. J. Med. Virol. 2017, 89, 1315–1322. [Google Scholar] [CrossRef]
  88. European Food Safety Authority. European Centre for Disease Prevention and Control the European Union One Health 2021 Zoonoses Report. EFSA J. 2022, 20, e07666. [Google Scholar]
  89. Rocheleau, J.-P.; Kotchi, S.-O.; Arsenault, J. Can local risk of West Nile virus infection be predicted from previous cases? A descriptive study in Quebec, 2011–2016. Can. J. Public Health 2020, 111, 229–238. [Google Scholar] [CrossRef] [PubMed]
  90. Casades-Martí, L.; Cuadrado-Matías, R.; Peralbo-Moreno, A.; Baz-Flores, S.; Fierro, Y.; Ruiz-Fonsac, F. Insights into the spatiotemporal dynamics of West Nile virus transmission in emerging scenarios. One Health 2023, 16, 100557. [Google Scholar] [CrossRef]
  91. Tsioka, K.; Gewehr, S.; Kalaitzopoulou, S.; Pappa, S.; Stoikou, K.; Mourelatos, S.; Papa, A. Detection and molecular characterization of West Nile virus in Culex pipiens mosquitoes in Central Macedonia, Greece, 2019–2021. Acta Trop. 2022, 230, 106391. [Google Scholar] [CrossRef]
Tropicalmed 08 00453 sch001
Scheme 1. The WNV Transmission Cycle: The virus circulates between vectors (mainly Culex spp. mosquitoes and the reservoir hosts; it accidentaly infects dead-end hosts (humans, equids).
Scheme 1. The WNV Transmission Cycle: The virus circulates between vectors (mainly Culex spp. mosquitoes and the reservoir hosts; it accidentaly infects dead-end hosts (humans, equids).
Tropicalmed 08 00453 sch001
Tropicalmed 08 00453 g001
Figure 1. Mean monthly climatic anomalies and hydrological variables of Greece for the years 2018–2023 and their comparison with the intensity of annual local WNV epidemics (a) for January, (b) April, and (c) July. Data were extracted from the Copernicus Climate Change Service/ECMWF. Circles correlate the big epidemics of 2010 and 2018 with the climatic variables.
Figure 1. Mean monthly climatic anomalies and hydrological variables of Greece for the years 2018–2023 and their comparison with the intensity of annual local WNV epidemics (a) for January, (b) April, and (c) July. Data were extracted from the Copernicus Climate Change Service/ECMWF. Circles correlate the big epidemics of 2010 and 2018 with the climatic variables.
Tropicalmed 08 00453 g001
Tropicalmed 08 00453 g002
Figure 2. Map of Greece with total numbers of human WNV cases throughout the 13.5-year period 2010–2023, by prefecture. White colour represents prefectures where no human cases were observed.
Figure 2. Map of Greece with total numbers of human WNV cases throughout the 13.5-year period 2010–2023, by prefecture. White colour represents prefectures where no human cases were observed.
Tropicalmed 08 00453 g002
Table 1. Factors affecting the intensity of WNV outbreaks in Europe.
Table 1. Factors affecting the intensity of WNV outbreaks in Europe.
Environmental FactorsReferences
Mean TemperatureWinterSpringSummer
Type of associationnegativepositivepositive[31,32,33,34,37,44]
Proposed mechanismaffects vector survival, depending on the vectorincreases biting rate, increases host-to-vector transmission probability, accelerates mosquito viral incubation period, potentially enhances oviposition activityaffects distribution, behaviour and survival of the mosquito vector, reduces incubation period in the competent vectors and affects host distribution and behaviour
very high temperatures reduce mosquito survival
Relative Humidity/PrecipitationWinterSpringSummer
Type of associationnegativepositive/negativenegative[34,36,45,46,47]
Proposed mechanismaffects vector survivalincreases the standing water resources at the beginning of the hot season/consequence of favourable higher temperatures- drought creates stagnant waterdrought leads to increases in mosquito numbers and increases biting rate
Ground Moisture/VegetationWinterSpringSummer
Type of associationpositive (when followed by a decrease in spring/summer)depending on mean temperaturespositive[43,46]
Proposed mechanismvariations influence the presence and size of the WNV vector populationsinconclusivefavours vector abundance[48]
Vector-Associated FactorsCurrent Situation in EuropeEffect on Potential Outbreak
Installation/availability of potent arthropod vectorsinstallation and endemicity in the Mediterranean Basin/Europe of Aedes mosquitoes, mainly albopictuspositive
(pros: very potent vectors, are able to infestate urbanized areas, bite throughout the daytime, contras: preferentially bite humans)		[49,50,51,52]
Hosts/reservoirsclimate change favours vector abundance, geographic location on the route of migratory birds from Africapositive[53]
Vector and viral overwinteringevidence of enzootic circulation, viral overwintering in non-migratory birds, evidence of viral overwintering in mosquitoespositive[23,24,54,55]
Socioeconomic FactorsCurrent Situation in EuropeEffect on Potential Outbreak
Economic crisiscoincided with the outbreak in 2010negative correlation of the Gross Domestic Product with WNV infections[56]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Kouroupis, D.; Charisi, K.; Pyrpasopoulou, A. The Ongoing Epidemic of West Nile Virus in Greece: The Contribution of Biological Vectors and Reservoirs and the Importance of Climate and Socioeconomic Factors Revisited. Trop. Med. Infect. Dis. 2023, 8, 453. https://doi.org/10.3390/tropicalmed8090453

AMA Style

Kouroupis D, Charisi K, Pyrpasopoulou A. The Ongoing Epidemic of West Nile Virus in Greece: The Contribution of Biological Vectors and Reservoirs and the Importance of Climate and Socioeconomic Factors Revisited. Tropical Medicine and Infectious Disease. 2023; 8(9):453. https://doi.org/10.3390/tropicalmed8090453

Chicago/Turabian Style

Kouroupis, Dimitrios, Konstantina Charisi, and Athina Pyrpasopoulou. 2023. "The Ongoing Epidemic of West Nile Virus in Greece: The Contribution of Biological Vectors and Reservoirs and the Importance of Climate and Socioeconomic Factors Revisited" Tropical Medicine and Infectious Disease 8, no. 9: 453. https://doi.org/10.3390/tropicalmed8090453

Article Metrics

Back to TopTop