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Climate change impacts on West Nile
virus transmission in a global context
rstb.royalsocietypublishing.org
Shlomit Paz
Department of Geography and Environmental Studies, University of Haifa, Israel
Review
Cite this article: Paz S. 2015 Climate change
impacts on West Nile virus transmission in a
global context. Phil. Trans. R. Soc. B 370:
20130561.
http://dx.doi.org/10.1098/rstb.2013.0561
One contribution of 14 to a theme issue
‘Climate change and vector-borne diseases of
humans’.
Subject Areas:
ecology, environmental science, health and
disease and epidemiology
Keywords:
vector-borne diseases, West Nile virus,
climate change
West Nile virus (WNV), the most widely distributed virus of the encephalitic
flaviviruses, is a vector-borne pathogen of global importance. The transmission cycle exists in rural and urban areas where the virus infects birds,
humans, horses and other mammals. Multiple factors impact the transmission and distribution of WNV, related to the dynamics and interactions
between pathogen, vector, vertebrate hosts and environment. Hence,
among other drivers, weather conditions have direct and indirect influences
on vector competence (the ability to acquire, maintain and transmit the
virus), on the vector population dynamic and on the virus replication rate
within the mosquito, which are mostly weather dependent. The importance
of climatic factors (temperature, precipitation, relative humidity and winds)
as drivers in WNV epidemiology is increasing under conditions of climate
change. Indeed, recent changes in climatic conditions, particularly increased
ambient temperature and fluctuations in rainfall amounts, contributed to the
maintenance (endemization process) of WNV in various locations in
southern Europe, western Asia, the eastern Mediterranean, the Canadian
Prairies, parts of the USA and Australia. As predictions show that the current trends are expected to continue, for better preparedness, any
assessment of future transmission of WNV should take into consideration
the impacts of climate change.
1. Climate change and vector-borne disease
Author for correspondence:
Shlomit Paz
e-mail: [email protected]
Climate change is a complex phenomenon [1] that affects human health. The
impacts are multifaceted and vary in scale and timing as a function of the
local environmental conditions and human vulnerability. As a part of that,
climatic change influences the emergence of vector-borne diseases such as
malaria, dengue and West Nile virus (WNV) by altering their rates, ranges, distribution and seasonality [2–7]. Vector-borne diseases are dynamic systems
with complex ecology, which tend to adjust continually to environmental
changes in multifaceted ways. Although climate is one of several factors that
influence the distribution of these diseases, it is known to be a major environmental driver influencing their epidemiology. Weather conditions (in particular
temperature, precipitation and humidity) affect the survival and reproduction
rates of the vectors, their habitat suitability, distribution and abundance.
Additionally, climatic factors impact the intensity and temporal activity of the
vector throughout the year and affect the rates of development, reproduction
and survival of pathogens within the vectors [5,8].
The Intergovernmental Panel on Climate Change (IPCC) [9] lists vectorborne diseases among the consequences most likely to change due to global
warming. Moreover, as these diseases are particularly sensitive to climatic fluctuations, they might serve as an alert to focus attention on climate change
threats [10,11].
The aim of this review is to examine and integrate the up-to-date knowledge
on the impacts of climate change on WNV transmission in a global context. All
available peer-reviewed studies that deal with linkages between climatic factors
and WNV have been collected for this paper, and most of them are mentioned
below. Special attention has been paid to recent publications that highlight
regional climatic change impacts on vector population dynamics and on
disease transmission.
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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2. West Nile virus
Multiple factors impact the complex epidemiology of WNV
besides its transmission and distribution. These factors are
related to the dynamics and interactions between the pathogen,
vector, vertebrate hosts and environment. Hence, among other
drivers, weather conditions have direct and indirect influences
on vector competence (the ability to acquire, maintain and
transmit the virus), on the vector population dynamics and
on the virus replication rate within the mosquito, which are
mostly climate- and weather-dependent [23,30,31]. Table 1
summarizes the main impacts of climatic variables on the
epidemiology of WNV.
(a) Temperature
Ambient temperature plays an important role in viral replication rates and transmission of WNV by affecting the length of
extrinsic incubation, the seasonal phenology of mosquito host
A common dogma in epidemiology is that above-average
precipitation might lead to a higher abundance of mosquitoes and increase the potential for disease outbreaks in
humans [51,52]. This pattern of a positive association with
rainfall in the months preceding disease outbreaks has
been demonstrated for WNV [42,53]. However, the literature
shows a more complex picture. Although the patterns of disease incidence can be influenced by the amount of
precipitation, the response might change over large geographical regions, depending on differences in the ecology
of mosquito vectors [23,52,54]. For instance, heavy rainfall
increases the standing water surface which is necessary for
mosquito larval development. On the other hand, heavy
rainfall might dilute the nutrients for larvae, thus decreasing
the development rate [55]. It might also lead to a negative
association by flushing the ditches and drainage channels
used by Culex larvae [56,57].
Below-average precipitation can facilitate population outbreaks of some species of mosquitoes because the drying of
wetlands disrupts the aquatic food-web interactions that
limit larval mosquito populations [44,56,58]. Drought leads
to close contact between avian hosts and mosquitoes
around remaining water sources and therefore accelerates
the epizootic cycling and amplification of WNV within
these populations [59]. Furthermore, during drought conditions, standing water pools become richer in the organic
material that mosquitoes need in order to thrive [22]. Such
water areas might be attractive for several bird species also,
which might increase the bird–mosquito interaction.
Phil. Trans. R. Soc. B 370: 20130561
3. West Nile virus and climate
(b) Precipitation
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West Nile virus is one of more than 70 viruses of the family
Flaviviridae of the genus Flavivirus. Serologically, it is a
member of the Japanese encephalitis serocomplex. The
viruses can be designated into at least five phylogenetic
lineages but only lineages 1 and 2 have been associated
with significant disease outbreaks in humans [12,13]. The
enzootic cycle is driven by continuous virus transmission to
susceptible bird species through adult mosquito blood-meal
feeding, which results in virus amplification. Species from
the genus Culex mosquitoes (family Culicidae) are the primary amplification vectors and also act as bridge vectors.
The transmission cycle exists in rural ecosystems as well as
in urban areas where the virus infects birds, humans,
horses and other mammals [14– 23]. The distribution of
WNV is dependent on the occurrence of susceptible avian
reservoir hosts and competent mosquito vectors, mosquito
host preference and availability of hosts [12].
Most human infections occur in the summer or early
autumn [24]. West Nile fever (WNF) is a potentially serious
illness for humans and approximately 1 in 150 infected
people develop a serious illness with symptoms that might
last for several weeks. Up to 20% of patients have milder symptoms and approximately 80% show no symptoms at all [25].
Geographically, the virus has circulated in Africa since
1937, and up until the early 1990s human outbreaks were
reported in Africa and Israel, mainly associated with mild
febrile illnesses. Since then, new viral strains, probably of
African origin, have increased human disease incidence in
parts of Russia and southern and eastern Europe, with
large outbreaks of increased clinical severity occurring in
Romania, Russia, Israel and Greece [12,26].
The first appearance of WNV in the western hemisphere
occurred in New York City in 1999 [27]. The virus had
spread to the Pacific coast by 2003 and to Argentina by
2005 [28,29]. Currently, WNV has an extensive distribution
throughout Africa, the Middle East, southern and eastern
Europe, western Asia and Australia, which derives from its
ability to infect numerous mosquito and bird species.
Today, as WNV is the most widely distributed of the encephalitic flaviviruses, it is a vector-borne pathogen of
global importance [12].
populations and the geographical variations in human case
incidence [22,30,32 –34]. Increased temperatures cause an
upsurge in the growth rates of vector populations, decrease
the interval between blood meals, shorten the incubation
time from infection to infectiousness in mosquitoes, accelerate
the virus evolution rate and increase viral transmission
efficiency to birds [22,23,30,32,35,36].
Laboratory experiments demonstrated that the virus is
capable of replication across a wide range of temperatures,
from 148C in poikilothermic mosquitoes [37] to 458C in febrile
avian hosts [33]. However, it was shown that the replication
cycle is completed more quickly in mosquitoes at higher
temperatures [38,39], while a clear association was found
between extreme heat and outbreak intensity in humans
[4,18,22,35,40– 43]. At the same time, it is important to note
that, in some cases, extremely high temperatures begin to
slow down mosquito activity. For example, temperatures
above 308C reduced larval survival of Culex tarsalis [44] and
slowed WNV growth in Culex univittatus [45].
In addition, the change in environmental temperatures
might have an indirect impact on the spread of the virus. It
is well known that the transmission cycle involves birds as
the principal hosts (and mosquitoes, largely bird-feeding
species, as the primary vectors) [23]. In recent years, it has
been observed that several bird species have been migrating
to their breeding grounds earlier as a result of an early rise
of the mean spring temperatures, which is one of the effects
of global warming [46–50]. This phenomenon might influence the appearance and timing of the disease in locations
near or along migration routes. However, this assumption
needs further investigation.
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Table 1. Impacts of climatic variables as drivers in the epidemiology of WNV.
impacts on the epidemiology of WNV
temperature
correlates positively with:
—viral replication rates
—seasonal phenology of mosquito host populations
—growth rates of vector populations
—viral transmission efficiency to birds
—interval between blood meals
precipitation
—incubation time from infection to infectiousness in mosquitoes
above average, floods
—leads to higher mosquito abundance
(contradictory
findings)
—reduces potential by flushing drainage channels used by Culex larvae
—correlates positively with potential for disease outbreaks in humans
below average, drought
—facilitates population outbreaks of some mosquito species
—‘rich’ standing water attracts several species of mosquitoes and birds; this increases the
bird – mosquito interaction and accelerates the epizootic cycling and amplification of WNV
within these populations
relative humidity
correlates positively with:
—vector population dynamics
—morbidity in humans
wind
contributes to virus spread by impact on wind-blown mosquitoes and on the arboviruses they transmit
affects bird migration through changes in the patterns of storm tracks
Moreover, ecological studies showed that drought conditions can facilitate population outbreaks of some species
of mosquitoes in the following year [58].
(c) Relative humidity
The research regarding the role of relative humidity in WNV
eruptions is very limited. Significant positive correlations
were found between hospital admission dates of patients and
relative humidity levels in the Tel Aviv metropolis (Israel)
[4]. A study in Maryland, USA, examined the effect of
off-season factors on mosquito population size. Among other
variables, the average maximum relative humidity was
associated with vector population dynamics [60]. A recent
analysis detected correlations between morbidity in humans
and weekly relative humidity in Europe and western Asia
[22]. All these studies found that air temperature is a better
predictor for increasing disease cases than air humidity.
(d) Wind
Wind patterns might contribute to virus spread by their
impact on wind-blown mosquitoes [61]. Storm fronts have
been proposed as dispersal mechanisms for mosquitoes
and the arboviruses they transmit [62 –64]. For example, it
was shown that wind is used by Culex tritaeniorhynchus
mosquitoes as a means of migration in China [65].
Winds might impact on WNV spreading also by affecting
bird migration through changes in the patterns of storm tracks.
In recent years, significant changes in the location and intensity of storms have been shown on a regional basis, as a part
of climate change observations and scenarios [66]. Thus, it
seems that change in storms might influence WNV dispersal
by impacting the dynamics of storm-driven birds [23].
The importance of climatic factors as drivers in the epidemiology of WNV is increasing under conditions of climate
change. Consequently, the aim of the following sections is
to highlight the linkages between climatic change and
WNV transmission in a global perspective (see also table 2).
4. Europe and Eurasia
(a) Main climatic change observations
Impacts of climate change vary by region, depending on the
change intensity and the vulnerability rate of the area. In
general, during recent decades Europe has warmed up; temperature rise was much larger than the global average,
especially in the north, and larger than the European average
in the mountain areas and the Mediterranean region. Over
the past 50 years, more frequent and more intense hot
extremes have occurred. This trend is expected to continue,
while predictions suggest a further temperature increase (of
between 2.58C and 4.08C) by the end of the century [67,68].
Changes in rainfall show more spatially variable trends
across Europe. Annual precipitation changes are already
exacerbating differences between the rainy northern part (an
increase of 10 –40% during the twentieth century) and the
dry southern region (a decrease of up to 20%). Heavy rain
events have increased in the past 50 years and are projected
to become more frequent. Dry periods are expected to increase
in length and frequency, especially in southern Europe.
Phil. Trans. R. Soc. B 370: 20130561
—geographical variations in human case incidence
correlates negatively with:
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climatic variable
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Table 2. The main climatic change observations (temperature and precipitation) in the study areas and their impacts on WNV transmission.
western
Asia
impact on WNV transmission
temperature increase
warmer conditions facilitated the establishment of WNV in new
increase in heat wave frequency and intensity
precipitation increase in the north and decrease (with dry
transmission
precipitation might increase standing water availability for
mosquitoes (but results for rainfall are less consistent)
in Eurasia and central Europe less summer precipitation
North America
and more river floods in winter
average temperature has risen
increased temperature is positively correlated with the rate of virus
evolution, with mosquito abundance and infection; it influences
WNV distribution and plays an important role in the
maintenance and amplification of human infection
across the USA precipitation has increased by an average
of about 5%
increase in water scarcity in the Canadian Prairies
Australia
annual average daily mean temperature has increased by
0.98C since 1910
findings are inconsistent, particularly when the analyses include
different vectors: in general, human outbreaks of WNV are
preceded by above average rainfall in the eastern USA and by
below-average rainfall on the western side
in a warmer climate, C. annulirostris populations are expected to
reach high levels of abundance earlier and maintain them for
longer
increased spring and summer monsoonal rainfall across
northern Australia and decreased late autumn and
an outbreak of equine encephalitis (WNVKUN) followed extensive
flooding across eastern Australia
winter rainfall across the south
Observations for Eurasia and central Europe show more temperature extremes, less summer precipitation, more river floods
in winter and higher water temperature [1,67,68]. The European Mediterranean region has become warmer with a
significant increase in the frequency, intensity and duration
of heatwaves [69,70] in parallel with a decrease in total precipitation. In this area, mutual enhancement ( positive feedback)
has been identified between droughts and heat waves [70].
(b) Climate change impact on West Nile virus
transmission
Since the mid-1990s, outbreaks in humans and horses have
been documented in Eurasia (Bucharest in Romania, the
Czech Republic, Hungary, and Volgograd in Russia), western
Europe (France, Italy, Spain and Portugal) and Israel. The lack
of cases in humans in northern Europe is possibly attributed to
the feeding behaviour of the predominant vector, Culex pipiens,
as well as to other factors, especially climate [71].
In 2010, large outbreaks occurred in northern Greece
(Macedonia), in Romania, Hungary, Italy and Spain, in
Russia (Volgograd), Turkey and Israel. These outbreaks in
humans were accompanied by infections in donkeys in Bulgaria and horses in Morocco, Portugal, southern Italy and
Greece. Since then, all subsequent years (2011 –2014) were
characterized by the re-emergence of WNV in Europe, with
human cases noted in almost all eastern, central and southern
countries [23,26,72].
The unprecedented upsurge in the number of human WNF
cases in summer 2010 was accompanied by extremely hot spells
in southeastern Europe and Eurasia [22]. According to the
World Meteorological Organization [73], this warming
peaked in this past decade ending in 2010, which was also
one of the three hottest years ever recorded. An analysis of
the climatic drivers of the 2010 outbreak found the ambient
temperature to be the most important [22]. The impact of climatic variables on the endemization of WNV in Europe and
western Asia has been reviewed recently by Paz & Semenza
[23]. They noted that in parts of Europe, climate change resulting in warmer conditions facilitated the establishment of WNV
in new areas through an expansion of range and seasonal abundance of vector species and by directly increasing competence
for transmission. These insights are reinforced by previous
studies from western Asia. A research about the linkage
between heatwaves and WNV upsurge in humans in Israel
showed that an early extreme rise in temperature in the hot
season is a good indicator of increased vector populations [4].
In addition, in their study on the outbreaks in the Volgograd
Province in Russia, Platonov et al. [31] showed that the abundance of Culex mosquitoes in an epidemic season is higher in
years with a mild winter and a hot summer.
Results for precipitation are less consistent. Papa et al. [74]
noted that increased rainfall and humidity (together with high
temperatures) have probably favoured the multiplication of
Culex species, leading to the occurrence of numerous cases of
WNV infection in humans in Central Macedonia in summer
Phil. Trans. R. Soc. B 370: 20130561
periods) in the south
more heavy rainfall events
areas through an expansion of range and seasonal abundance of
vector species, and by directly increasing competence for
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Europe and
main climatic changes
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5. North America
Impacts of climate change in North America differ by region,
with coastal areas, mountains and flood plains being particularly vulnerable. Generally, during the past 50 years, the
average temperature across the USA has risen, while precipitation has increased by an average of about 5%. Some
extreme weather events, such as heat- and cold-waves,
intense precipitation events and regional droughts, have
become more frequent and intense [75– 77].
Northwards, Canada has already experienced warming
that is disproportionate to global climate change, with average temperatures in some northern regions increasing by
more than 28C. In the Canadian Prairies (where WNV is a significant concern) increase in water scarcity has been observed
in parallel with warmer and drier summers [78,79].
The IPCC projects that climatic and weather conditions in
North America in the coming decades are likely to include
warmer temperatures, shorter winters, increased proportion
of precipitation falling as rain rather than snow, increased frequency of heavy rainfall and other extreme weather events.
These changes pose risks to public health including the
emergence of vector-borne diseases [1,70,77].
(b) Climate change impact on West Nile virus
transmission
WNV was first reported in North America in New York City
in 1999, when it infected many species of birds as well as
humans and other mammals [36]. Later, the virus moved
across the continent, reaching Canada and Central America
by 2002 and was isolated in California in July 2003 [80]. In
fact, WNV became endemic across most temperate regions
of North America [12].
The effects of weather fluctuations on WNV transmission
in the USA and Canada have been analysed by several
researchers who showed that increased temperatures influence North American WNV distribution and play an
important role in the maintenance and amplification of
human infection [43,81]. Soverow et al. [42] assessed 16 298
human WNF cases from 2001 to 2005 across 17 states in the
USA. They found positive associations with increasing temperature over each of the four weeks prior to symptom onset.
Specifically, an increase of 58C in the mean maximum weekly
temperature was associated with a significant 32–50% higher
incidence of reported WNF infection.
In a study in Georgia, temperature was found to be
among the most important variables in predicting the distribution of WNV [82]. Warm temperature was associated
statistically with higher human infection risk in Connecticut
[83], with the virus spread into western states and with
county-level mosquito infectivity in California [32].
Higher winter temperatures and a warmer spring might
lead to larger summer mosquito populations [60]. In their
5
Phil. Trans. R. Soc. B 370: 20130561
(a) Main climatic change observations
study in Illinois, Kunkel et al. [39] showed a correlation
between the number of days when daily maximum temperature exceeded a threshold, the timing of a seasonal shift to a
higher proportion of C. pipiens among all Culex species, and
the onset of the amplification phase of seasonal WNV
transmission.
In a modelling research in the urban landscape of Chicago,
spatial and statistical techniques were used to analyse and forecast fine-scale spatial and weekly patterns of WNV mosquito
infection relative to changing weather conditions. The temperature was found to be the main factor that mediates the
magnitude and timing of the increased minimum infection
rate within the season. It was also strongly indicated as a key
factor for explaining much of the observable differences between
years while the effect of increased temperature on minimum
infection rate was especially strong within a week [36].
Temperature has been linked to the rate of virus evolution. A more quickly replicating virus spurred by warmer
conditions precedes an increase in mosquito infection
[59,84]. It was detected that warmer temperatures facilitated
the displacement of the WNV NY99 genotype by the WN02
genotype [30]. In a study in suburban Chicago, Bertolotti
et al. [85] discovered high genetic variation of WNV at
fine temporal and spatial scales, while variation in local
temperature was offered as one explanation for this.
As the impact of precipitation in WNV transmission is
more indirect, the findings regarding North America are inconsistent in particular when the analyses include different vectors
[36,42,86]. For instance, the population size of C. pipiens (the
primary enzootic and epidemic vector in the eastern USA
north of 368 N) is often impacted negatively by large rain
events due to the flushing of catch basins [57]. By contrast,
the vector C. tarsalis generally responds positively to heavy
precipitation, which provides the typical larval habitat in
rural areas in the western part of the USA [87,88].
Regional trends showed that prior drought contributed to
the initial USA WNV outbreak [86,89]. Drought conditions
can increase the abundance of some vector populations in
semi-permanent wetlands as they result in more larval breeding sites with fewer competitors and mosquito predators [58].
In Florida, spatial and temporal differences in periods of
drought and rain were associated with human WNF cases
and infection of sentinel chickens. Springtime drought followed by a wet summer was found to be a good predictor
of WNV incidence in humans. Close proximity of birds and
mosquito vectors during times of drought was detected as
responsible for the increased virus transmission [56,59,84].
Using county-level precipitation and human WNV incidence data (2002–2004), Landesman et al. [52] tested the
impacts of above- and below-average rainfall on the prevalence
of WNF in human populations both within and between years.
Although the mechanism is not fully understood, the authors
found evidence that human WNV incidence is most strongly
associated with annual precipitation from the preceding year
and noted that human outbreaks of WNV are preceded by
above-average rainfall in the eastern USA and by belowaverage rainfall on the western side in the previous year. In
the western USA, primary vectors of WNV include species
such as C. tarsalis [90], which are likely to undergo outbreaks
following years of low rainfall as a result of changes in foodweb structure. As the abundance of mosquito larvae is often
limited by predators and competitors, in years following a
drying event, both efficient mosquito predators and mosquito
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2010. Paz et al. [22] did not detect significant linkages between
rainfall amounts and WNV cases in the region; however,
they noted that three infected sites—Trapany (Sicily, Italy),
Campobasso (Molise, Italy) and Thessaloniki (Greece)—were
rainier than usual in July. Precipitation in these areas might
have increased the standing water availability, which is an
important breeding resource for mosquitoes.
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(a) Main climatic change observations
The Australian continent is characterized by climate variability. Overall, each decade in Australia since the 1950s has been
warmer than its predecessor, while the annual average of the
daily mean temperature has increased by 0.98C since 1910. A
general trend towards increased spring and summer monsoonal rainfall across northern Australia and decreased late
(b) Climate change impact on West Nile virus
transmission
The Kunjin virus (WNVKUN), which is spread by the bite of
infected mosquitoes, is the Australian subtype of WNV. The
main mosquito associated with the virus spread is Culex
annulirostris that breeds in fresh water environments.
Although only a small number of cases are reported annually,
the virus is known to occur in many parts of Australia, particularly in the tropical northern regions. WNVKUN is less
virulent than the current USA strain of WNV. Infection
rarely causes disease in humans and most infected people
do not develop any symptoms [98,99].
In 2011, a highly pathogenic strain caused an unprecedented
outbreak of acute equine encephalitis leading to the isolation of
the first virulent strain of WNVKUN. This eruption followed
extensive flooding across eastern Australia that promoted
ideal conditions for freshwater C. annulirostris mosquito breeding [100]. Indeed, these mosquitoes require an increase in
precipitation amount to ensure larval habitat and to maintain
humidity for adult survival [101].
In addition, changes in temperature affect the transmission of WNVKUN. In a warmer climate, C. annulirostris
populations are expected to commence activity and reach
high levels of abundance earlier, and maintain them longer.
The season of arbovirus activity might be prolonged, with
potential transmission increase [101]. Moreover, as a result
of temperature increase, the vectors are expected to move
further south into currently cooler regions because summer
temperatures in southern areas will be more adequate for
initiating and maintaining the virus amplification [102,103].
7. South America
The recent IPCC report [1] indicated an overall increase in
warm days and heatwaves in South America, and more
regions where more precipitation increase than decrease
was observed, with spatially varying trends. However,
owing to lack of data and studies in South America, there
is medium to low confidence regarding climate change
observations in the continent [104].
Studies on the impact of climate change on WNV spreading
in South America are limited. The southward dissemination of
WNV into the Caribbean and Central and South America is
attributed to migratory birds. WNV was first detected in 2001
in Jamaica and the Cayman Islands. Cross-reactive WNV antibodies in humans have been detected in Mexico, the Bahamas
and Cuba [105]. In 2006, four serologically confirmed human
WNF encephalitis cases were reported in Argentina [106]. Serologic evidence of WNV infection in horses was reported in
Guadalupe, Mexico, Puerto Rico and Colombia. Resident
birds tested positive for antibodies to WNV in the Dominican
Republic and Venezuela [105]. Recently, WNV antibodies
were identified in several horses and birds in Brazil [107].
Although extensive, the spread has not been accompanied by
notable avian mortality or disease in humans or horses in
Latin America and the Caribbean [71], although the main concern is the absence of data on the disease burden in people,
horses or birds [108].
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Phil. Trans. R. Soc. B 370: 20130561
6. Australia
autumn and winter rainfall across the south have been
observed [97].
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competitors are rare [58]. Instead, many of the important WNV
vectors in the eastern USA (e.g. C. pipiens, Culex restuans) breed
in natural and artificial containers [14] where increased rainfall
might lead to a larger population of overwintering mosquitoes
by increasing the number of available larval habitats [52].
In a large study in the USA, one or more days per
week of heavy precipitation (defined as greater than or
equal to 50 mm in a single day) were associated with a 33%
higher incidence of reported WNV infection during the
same week, while the incidence remained elevated in the
subsequent two weeks [42].
According to the Centers for Disease Control and Prevention
(CDC) [91], the recent unusually mild winters, early springs and
early summers aided transmission of the virus in Texas in the
summer of 2012. This outbreak was attributed in part to drought
conditions, which reduced water flow and created stagnant
water pools ideal for breeding mosquitoes [92].
As mentioned in §3(d), it has been proposed that winds
serve as dispersal mechanisms for mosquitoes and the arboviruses they transmit. Reisen et al. [64] mentioned that high
barometric pressure conditions over Nevada during the
summer of 2003 created a persistent clockwise airflow pattern
from Colorado into southeastern California through Arizona
and northern Mexico. They suggested that, based on surveillance in Arizona during 2003, which detected WNV in
concurrence with that in southeastern California, it is reasonable to assume that a climate-driven mechanism brought the
virus south-west from the Colorado epicentre.
In Canada, WNV is a significant concern for public health
and wildlife conservation in the Canadian Prairies, one of the
most highly endemic regions in North America [93]. In that
region, the mosquito species C. tarsalis Coquillett, whose distribution is determined by temperature and precipitation [94],
is the principal vector for WNV [95].
Laboratory experiments demonstrate that the temperature
threshold for survival of C. tarsalis is generally between 148C
and 358C, and within this range, temperature is positively correlated with the development rate of the vector [44,96]. In a
recent study, Chen et al. [93] integrated empirically derived,
biologically relevant temperature thresholds for C. tarsalis survival and WNV development, using statistical models to
predict the effects of climate change on the distribution and
abundance of C. tarsalis and WNV in the Canadian Prairies.
Their results suggest that the predicted mean monthly temperatures will not exceed the upper threshold for survival of
adult female C. tarsalis, whereas the temporal and spatial distribution of WNV will remain determined primarily by the lower
temperature limitation for WNV amplification. The authors
expect that elevated temperatures will increase the infection
rate of WNV in C. tarsalis, especially in the southern part of
the Canadian Prairies without a compensatory increase in
mosquito mortality [93].
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Table 3. Examples of recent statistical models that aim to predict WNV transmission/dynamics based on climatic predictors.
study area
study aims to predict:
the most important predictor
Shaman et al. [56]
mosquito collection from
mosquito (Aedes vexans, Anopheles
surface wetness, positively associated with
northern New Jersey and
meteorological data for
Walsh et al. [60]
Allentown, PA, USA
Maryland, USA
walkeri and C. pipiens)
abundance
mosquito (Aedes sollicitans and
Culex salinarius) population size
A. vexans and Anopheles walkeri,
negatively associated with C. pipiens
temperature variables—average maximum
minimum temperature below freezing
during the winter months were
predictive of mosquito populations
Epp et al. [111]
province of Saskatchewan,
Canada
risk of WNV in humans
higher temperatures overall and decreasing
rainfall into July
Ruiz et al. [36]
urban landscape of Chicago,
fine-scale spatial and weekly
increased air temperature was the
USA
patterns of WNV mosquito
(C. pipiens and C. restuans)
strongest temporal predictor
infection relative to changing
weather conditions
Chen et al. [93]
Canadian Prairies, Canada
effects of climate change on the
distribution and abundance of
temperature increase
C. tarsalis and WNV
Tran et al. [112]
Europe and neighbouring
countries
WNV risk in humans
anomalies of temperature in July, Modified
Normalized Difference Water Index in
early June, presence of wetlands,
location under migratory routes and
occurrence of a WNF outbreak in the
previous year were identified as risk
factors
8. Discussion
The recent Fifth Assessment Report of the IPCC [1] presents
stronger evidence than previously that multiple components
of the Earth’s climate system are changing. Global average air
temperature has risen by around 0.858C since 1880 and each
decade has been warmer than its predecessor [1]. Although
climate change impacts vary by region, it is well established
that it influences the distribution of vectors, pathogens of
vector-borne diseases and the habitat suitability for vectors.
Climate change also contributes to the expansion and shifting
of endemic regions [10,109].
WNV is the most widely distributed known arbovirus in
the world. The factors that explain this extensive distribution
are complex and include the interactions between the vector,
virus and host as well as climatic factors. Changes in climatic
patterns affect WNV transmission directly through relations
between the pathogen, host and vector (e.g. virus replication
rate within the mosquito), and indirectly via changes in ecosystem characteristics (such as water temperature).
According to Reisen et al. [32], WNV tended to disperse
into new areas during years with above-normal summer
temperatures while the amplification during the following
year occurred in summers with above-normal or normal
temperatures. This insight was evidenced recently in
Europe and western Asia, when the outbreaks in the summers of 2011–2013 occurred in most of the same disease
locations as in 2010, which was an extremely hot year
[22,72]. Another example appeared in the northern USA
when the increasing occurrences of warmer weather patterns
lead to increased incidence of WNV infections [110].
Based on the above review, it is suggested that recent variations in climatic conditions, particularly increased ambient
temperature and fluctuations in rainfall amounts, contributed
to the maintenance (endemization process) of WNV in various
locations in southern Europe, western Asia, the eastern Mediterranean, the Canadian Prairies, parts of the USA and
Australia. Limited knowledge is available regarding climatic
changes in South America and Africa. However, based on
the aforementioned insights, it is reasonable to expect that
global and continental warming will contribute to the risk of
WNV outbreaks in these continents also.
Despite the existence of surveillance systems in several
countries, outbreaks appear to be temporally and spatially
unpredictable [55]. The prediction of WNV spread and eruption is challenging as it propagates via a complex of
interrelationships. This notwithstanding, several statistical
and mathematical models have recently attempted to predict
Phil. Trans. R. Soc. B 370: 20130561
temperature, total heating degree-days
and the total number of days with a
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reference
7
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9. Conclusion
Recent climatic changes, particularly the increase in ambient
temperature and fluctuation in rainfall amounts, have contributed to the endemization of WNV in various locations
around the world. As predictions show that the current
trends are expected to continue, for better preparedness,
any assessment of future transmission of WNV should take
into consideration the impacts of climate change.
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