Focus Article
West Nile virus, climate change, and circumpolar vulnerability Kara C. Hoover1* and Christopher M. Barker2,3 Edited by Timothy R. Carter, Domain Editor, and Mike Hulme, Editor-in-Chief
Climate has strong impacts on the spatial ranges of vector-borne infectious diseases as well as the timing and intensity of disease outbreaks; these and shifting challenges to human health driven by future climate change are critical concerns. Many diseases of tropical origin, including West Nile virus (WNV), are sensitive to climate and likely to change their distributions in the coming decades. The 1999 outbreak of WNV in North America is an example of rapid viral adaptation to a new geographic area while recent outbreaks in Europe demonstrate the capacity of multiple viral strains to expand rapidly. WNV is one of the most widely distributed arboviruses and has displayed high rates of mutability, adaptability, and virulence. Northward expansion of WNV is happening in Europe and North America and may make WNV an increasingly worrying health risk at higher latitudes. Circumpolar northward expansion of WNV’s enzootic range appears unlikely over the coming century—at least for sustained enzootic transmission—but isolated and ephemeral transmission events might occur if the virus were to be introduced by migrating birds during warm months. Human populations in this area are at greater risk for health impacts from WNV transmission due to limited healthcare in rural areas, higher underlying morbidity in indigenous populations, and prolonged human-environment interactions (in populations engaging in traditional lifestyles). This review presents a multidisciplinary synthesis on WNV and climate change, potential for WNV expansion, and the vulnerability of the circumpolar north. © 2016 Wiley Periodicals, Inc. How to cite this article:
WIREs Clim Change 2016, 7:283–300. doi: 10.1002/wcc.382
INTRODUCTION
S
ince its well-documented arrival and spread across much of the western hemisphere,1 West Nile virus (WNV) has remained an important public health concern and is now the leading cause of arbo-
*Correspondence to:
[email protected] 1
Departments of Anthropology/Chemistry and Biochemistry, University of Alaska Fairbanks, Fairbanks, AK, USA
2
Department of Pathology, Microbiology, and Immunology & Center for Vectorborne Diseases, University of California, Davis, CA, USA
3
Fogarty International Center, National Institutes of Health, Bethesda, MD, USA Conflict of interest: The authors have declared no conflicts of interest for this article.
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viral encephalitis in the United States. In the United States alone, it has caused nearly 41,642 reported cases of human disease and 1752 deaths since its arrival in 1999, including 5674 cases and 286 deaths during a widespread outbreak in 2012.2 The virus was introduced to Central Europe from Africa via the Middle East in 1999 (and again in 2000 to Russia) and was limited to local outbreaks3; in 2008, the virus spread rapidly in Europe and has since been associated with hundreds of neuroinvasive cases in Hungary, Greece, and Serbia.4 – 9 The virus is maintained in transmission cycles between bird-feeding mosquitoes (primarily in the genus Culex) and various species of wild birds.1,10,11 The vectors and hosts—and indeed the WNV pathogen itself—are affected by climate in a number of ways.12 The availability of water influences WNV
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transmission indirectly via changes to population dynamics of mosquitoes and birds and of humans and birds13 – 16; some evidence suggests that ticks may serve as reservoirs but are not major vectors.17,18 Temperature fluctuations markedly alter the rate of viral replication in mosquito vectors and developmental rates of immature mosquitoes, as well as the timing of annual emergence from overwintering sites at temperate latitudes.14,19 – 22 These factors collectively affect the potential for WNV transmission and ultimately the risk of infection in the human population. Various hypotheses and anecdotal evidence have been offered to explain the impacts of climate on WNV transmission, particularly in relation to conditions that result in outbreaks, and some studies have considered this topic in some detail.21,23 – 25 We focus on the climatic influences that define WNV’s current spatial limits (i.e., range of occurrence) and intensity (i.e., sizes of outbreaks), then consider how these may be altered as the climate continues to change and what the consequences for Arctic regions might be in response to those changes.
OVERVIEW OF WNV TRANSMISSION First documented in the West Nile subregion of Uganda in 1937,26 WNV is an enzootic, neurotropic flavivirus from the Japanese encephalitis group within the family Flaviviridae.27,28 The virus is transmitted by mosquitoes1,29 – 33 and amplified in avian hosts.30,34 – 36 Human infection occurs tangentially to bird-mosquito amplification cycles and is often caused by biting of competent bridge vectors (commonly, mosquitoes that feed on birds and mammals, such as Culex pipiens, Culex tarsalis, and Culex modestus)35,37,38 and potentially other competent mosquitoes that bite a diverse range of hosts such as Aedes albopictus.31 The virus is maintained by birds (particularly perching birds in the order Passeriformes)39 and
various species of mosquitoes (typically bird-feeding Culex species). Birds serve as amplifying hosts and mosquitoes serve as vectors that transmit the virus between birds35 (Figure 1). Viremias in hosts and the resulting differences in host competence, particularly among species, are important factors in WNV transmission and outbreaks.34,39 The most important mosquito vectors in North America vary regionally and according to local ecological context but include C. pipiens, C. quinquefasciatus, and C. tarsalis.29 – 31 Primary European vectors are C. pipiens and C. modestus.40– 42 Numerous other mosquito species may become infected with WNV through feeding on competent hosts, but efficient transmission requires the mosquito to acquire the virus from an infectious host and pass it on to another competent host to perpetuate the cycle.29,30,35 The complex multihost, multivector transmission cycles of WNV result in strong geographic and temporal heterogeneity in transmission. Host diversity may limit the virus, a phenomenon known as the dilution effect. Biodiversity of vertebrate hosts is linked to lower incidence of infection because the virus is diluted by mosquito feeding across multiple species (many of which are likely to be poor reservoirs for WNV) rather than concentrated on one or a few competent hosts.43 – 45 Vector feeding is not random and expectations based on host diversity alone are strongly altered by host availability during mosquito-feeding periods and vector-feeding preferences that may focus biting on a few host species even in the presence of high diversity. When vectorhost contact rates favor highly competent avian hosts, viral amplification intensifies.34,36,46 WNV has two main lineages,47 with three to five additional proposed lineages.48 – 50 Lineages 1 and 2 share approximately 75% of their nucleotides but there is a clear distinction in the lineages in terms of geographic range and impact on health: Lineage 1 viruses have been associated with high mortality (primarily among equines and birds) and a higher degree of neuroinvasiveness in mouse models; until
F I G U R E 1 | Schematic showing the West Nile virus transmission cycle between Culex mosquitoes and several representative species of passerine birds, with tangential transmission to humans and horses, which are dead-end hosts.
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recently, Lineage 2 viruses were limited to subSaharan Africa and Madagascar and have not been associated with severe human illness.51 The majority of documented human and animal disease cases have involved strains in Lineage 1, which has expanded its distribution from the Old World tropics to include much of the globe during the past 15 years. Multiple Lineage 1 strains have emerged in North America due to virus evolution since 1999.52 Infection of humans and other animals with Lineage 2 also has been reported in Europe since 2004,6,53 – 55 with phylogenetic analysis indicating two separate introductions of Lineage 2 strains from Africa to Eurasia: Central Europe in 1999 and Russia in 2000.3 Increased viremia and mortality in American crows have been linked to a single amino acid change in the NS3 protein.56 A substitution at the same location in a Lineage 2 strain was also found in an outbreak of neuroinvasive disease in Greece in which 17% of cases had resulted in death.55 Mutations in the NS3 protein may be selected in multiple lineages due to its role in increasing the rapidity of virus assembly which diminishes the ability of the host immune system to neutralize the viral infection.57,58 Overall, most humans infected with WNV do not have symptoms of disease, but around 20% experience a febrile illness and 1% experience more severe neuroinvasive disease.59,60 West Nile fever symptoms include headache, vomiting, fatigue, weakness, nausea, and rash. The virus may infect diverse cell populations and cross the blood–brain barrier to replicate in neuronal cells, progressing to the neuroinvasive form (e.g., meningitis, encephalitis, and/or acute flaccid paralysis).61 – 63 The likelihood of developing severe illness increases in elderly individuals. There is no treatment for WNV infection other than symptomatic treatment.64 WNV-vaccine approaches are in development for humans but have yet to reach clinical trials. Immunotherapy experiments on mouse models indicate limited success,65 but eliciting a protective immune response in elderly or immunocompromised target populations presents a major challenge, and clinical trial locations are difficult to define given the low incidence of disease and geographic focality of WNV transmission.66
ENVIRONMENTAL DRIVERS Seasonal Variation Mild winters have been associated with increased WNV activity in several studies.12,23,67,68 The exact mechanism by which WNV transmission would be increased by a mild winter (or conversely, decreased
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by unusually cold winters) is not known. Mild winters may result in lower-than-normal mosquito and resident bird mortality,69 and a spring with strong avian reproductive success enabled by favorable climate could increase the number of susceptible hosts and in turn diminish any impact of herd immunity following a year with intense WNV activity.70,71 The degree to which avian reproductive success would alter WNV-transmission potential in most years is likely to be smaller than that of mosquitoes. An adequate number of competent hosts certainly is essential for transmission to proceed, but there is little evidence that the availability of avian hosts as bloodmeal sources limits vector poulations. Aquatic immature dynamics of mosquitoes are probably a greater limitation on population size. Also, the rate and scale of variation in population density is much greater for vectors than hosts. Warm winter and spring conditions also could enable an early start to transmission and allow added time for WNV amplification in bird-mosquito cycles, potentially setting up increased risk for outbreaks of human disease. However, the highest incidence of human WNV disease in the United States has been in the northern Great Plains, where spring arrives relatively late and mosquitoes emerge from diapause later than in southern locales. In these areas, any climate-related delays in annual initiation of transmission must be overcome by efficient amplification aided by rapid warming upon the arrival of spring, combined with high competence of C. tarsalis as a vector.29 – 31 In Europe, important environmental factors are proximity to wetlands and migratory routes for birds, high temperatures during summer, and anomalies in surface water in late spring.72
Heat Waves Above-normal temperatures have been among the most consistent factors associated with WNV outbreaks. This has been found in both the Americas and Europe, for both of the main WNV Lineages 1 and 2.20,23,67,73,74 Extremely high summer temperatures were linked in 2010 to an increase in WNV cases in Europe.73 In areas where WNV can survive the winter or be reintroduced through vector or host movement, the degree to which WNV is amplified during late winter and early spring is a critical determinant of whether summer outbreaks will occur. At temperate latitudes, periods of warm weather following the winter solstice trigger the emergence of female mosquito vectors from diapause,22,75,76 which can result in an early start to the mosquito season, or in some cases, could lead to
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higher mortality because of premature consumption of fat reserves or emergence during times when cold temperatures are likely to resume.77 Early amplification of WNV between birds and mosquitoes during spring could increase the probability of outbreaks, and temperature is a key limiting factor for transmission during the early part of the transmission season. Laboratory experiments,19,20,78,79 correlative studies,14,23,80 – 85 and theoretical models21,86 alike have suggested that warm temperatures enhance mosquito population sizes and the efficiency of WNV transmission. The effects of temperature are primarily through acceleration of physiological processes within poikilothermic (cold-blooded) mosquitoes, which results in faster larval development and shorter generation times,19 more frequent mosquito biting,87 and shortening of the extrinsic incubation period,20,79 which is the time required for infected mosquitoes to transmit WNV. These accelerated rates respectively lead to more infected vectors, increased contact between mosquitoes and hosts, and larger numbers of vectors surviving to transmit WNV. The temperature dependencies described for early amplification also apply in summer, and summer is the period when WNV outbreaks can occur in humans following amplification in enzootic cycles. In the warmest areas, summer temperatures permit relatively efficient transmission during average or even cooler-than-average years, but WNV transmission intensifies at higher temperatures and most outbreaks have occurred during periods of unusual warmth. Above-normal temperature anomalies have delineated outbreaks in both North America and Europe and may be implicated in regional persistence over the winter.6,20,88,89 For example, a 5 C increase in mean maximum weekly temperature was associated with a 32–50% increase in WNV infection cases in the United States during 2001–2005.74
Drought The relationship between WNV amplification and water supply is quite complex, and some studies have found drought to be a key precursor or cofactor in WNV epidemics,16,90,91 although outbreaks in Eurasia and North America have followed both unusually dry and unusually wet conditions.74,89,90 Particularly in urban areas, extended periods of drought can result in increased mosquito abundance that may enhance transmission. Such conditions occur because urban stormwater management systems are not regularly flushed by rainwater during droughts, and instead they are supplied with regular water inputs 286
from landscape irrigation systems mixed with enough organic matter to provide ideal mosquito habitat.92,93 The particular sequence of drought and wetting leading up the summer transmission season also appears to be important, but the findings vary among studies and geographical regions. In Florida, conditions for WNV outbreaks have been associated with spring drought followed by a wet summer,16 and a national study also found antecedent wet conditions to be associated with intensified WNV activity in the eastern United States, while the opposite was true in the western United States.90 In Colorado’s eastern plains, wet springs followed by dry summers led to increases in human WNV-disease incidence,85 and the very large outbreak centered around Dallas, Texas in 2012 occurred when an unusually wet winter was followed by summer drought.23 Droughts may lead to outbreaks due to an increase in the abundance of certain species of Culex (such as C. pipiens)82 and the concentration of avian hosts and vector mosquitoes around remaining water sources.16
CLIMATIC LIMITS OF WNV’s RANGE The range of WNV’s existence, like that of other vector-borne pathogens, is limited by climate. As discussed above, climate may affect WNV directly (e.g., by limiting its rate of replication) or indirectly through impacts on host or vector populations that affect the sustainability of transmission. Perhaps the most obvious climatic factor that limits WNV transmission is cold temperature. There is a lower limit for temperatures below which viral replication cannot proceed, and this defines the absolute limits for transmission by poikilothermic (variable internal temperature) mosquitoes. Laboratory results at constant temperatures have shown that temperatures must remain above ≈14 C for viral replication in Culex vectors,20,79 but more research is needed to understand how the effects of natural diurnally cycling temperatures may differ from those at constant temperatures in the laboratory, as shown for other mosquito-borne pathogens.94 – 96 Temperatures are colder and winters are harsher at higher latitudes and elevations,97,98 and both serve to constrain the potential for transmission of WNV and other vector-borne pathogens. The environmental niche of WNV’s mosquito vectors appears to be broader than that of WNV itself,99 but for diapausing (i.e., hibernating) female mosquitoes during winter, mortality has been shown to increase as temperatures approach the freezing point.100 – 103 This would reduce the number of mosquitoes
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available to initiate transmission to avian hosts as the weather warms, and if these mosquitoes are also vertically infected (from mother to offspring) with WNV, mortality from winter cold could sharply reduce or eliminate the reservoir of infectious vectors that enable the virus’s persistence through winter. Such a tenuous carryover between years at the margins of WNV’s range may cause stochastic fadeout in most winters, requiring a reintroduction of virus from other locations to reinitiate local transmission cycles. Hot, dry climates such as those in the southwestern United States may limit WNV transmission in the absence of anthropogenic influences, primarily due to constraints on vector and host population dynamics. Irrigation can alter natural habitat availability, providing water sources for mosquitoes and birds that transmit WNV, potentially with a reduction in the abundance of vectors in midsummer in the hottest deserts due to diminished availability of surface water.104 The shallow water bodies inhabited by immature WNV vectors frequently reach temperatures that equal or exceed daytime air temperatures,105 and such temperatures have been shown to increase mortality sharply in immature mosquitoes.19,106 Extreme summer temperatures are not likely to have direct negative effects on WNV-replication rates in mosquitoes, even in hot climates (e.g., with daily air temperatures reaching 41–44 C). Such temperatures have been shown to limit replication of some WNV strains in the laboratory,107 but WNV-infected adult mosquitoes are not exposed regularly to such extreme temperatures because they avoid the peak daytime heat by taking shelter in cooler microhabitats during the day, emerging to seek bloodmeals during evening and nighttime hours.108 Also, the normal to febrile range for avian body temperatures is approximately 40–45 C, meaning that the virus must maintain the ability to replicate at these temperatures during each mosquito-bird transmission cycle.109 Precipitation probably plays a smaller role in defining WNV’s range than it does in driving interannual variation in WNV’s transmission intensity. Nevertheless, the availability of water is important because it defines land cover and land-use patterns, which in turn affect the composition of host and vector communities.24,81 In areas with low precipitation and intense heat such as deserts, surface water evaporation rates are high and habitats for aquatic stages of WNV vectors are limited, although irrigation may provide habitat in otherwise arid regions, thus altering natural seasonal vector abundance patterns.104 The northern limits of WNV’s range in North
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America correspond approximately to limits of agricultural and urbanized areas, both of which provide the most important aquatic habitats for the Culex mosquitoes that transmit WNV.104,110 – 112
POTENTIAL FOR RANGE EXPANSION WNV is now found on every continent except Antarctica, and its broad distribution and potential for spread have been among its hallmarks. Recently emerged strains that have more severe pathogenicity in hosts56,113 represent a subset of the total WNV range. Prior to 1996, WNV already had a broad distribution that included Africa, southern Europe, the Middle East, western Asia, and north to western Russia. Despite its broad range, it had received relatively little attention, primarily because the disease cases it caused were relatively mild.114 Beginning in 1996, however, WNV began to receive more attention because of a large outbreak around Bucharest, Romania that was notable for its occurrence in a densely populated urban area with a high incidence of neuroinvasive disease.8 In the Mediterranean region, there was an increased frequency of WNV outbreaks beginning in the mid-1990s in horses and humans across several countries including Algeria, Morocco, Tunisia, Italy, Israel, and France.115 The trend has continued through to the present.5,6,54,116,117 The Czech Republic represents the northern limit of the virus in Europe at 48 470 N.9 Predictions for the future of WNV in Europe are unclear beyond the fact that the virus is now endemic in many areas,4,7 apparently with the aid of frequent reintroduction in locations along major bird migration routes.118 Persistent human infection is expected. The climate in much of Europe is suitable for WNV persistence,24 and Culex vectors such as C. pipiens and C. modestus are also broadly distributed.40,41,119,120 Latitudinal limits for endemic and ephemeral transmission in Europe appear to be similar to those in the Americas.121,122 Migratory birds appear to provide an important means for viral movement, both from Africa into Europe and southward from Europe back into Africa,24,123 – 125 and they will likely continue to enable its spread into new areas. WNV was found in the Americas for the first time in 1999. Following its arrival in New York, WNV’s expansion westward and southward across the continent was dramatic and unprecedented.1 The virus expanded its range in the region surrounding
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New York in 2000 and had spread south into the Caribbean Basin by 2001.126 The Rocky Mountains did little to slow its westward advance, and it had reached western Colorado, Idaho, and Washington by late 2002, and California during the summer of 2003.127,128 The virus simultaneously continued its spread southward, reaching Mexico in 2002 and eventually Argentina by 2004, along with many other countries in the interim.126,129,130 Phylogenetic analyses have shown that Mexican, Caribbean, and Central American isolates have been the result of viral spread from the United States.131 but recent analysis has suggested that 2006 isolates from Argentina could have been the result of delayed detection of an independent, earlier introduction from the Mediterranean region.132 Expectations following WNV’s early spread in North America were that the tropics, with warm year-round temperatures, could be very receptive for WNV and potentially serve as a reservoir from which WNV could be reintroduced into North America by migrating birds. WNV’s present distribution spans the Americas, from mid-latitude Canada south to Argentina and nearly everywhere in between. However, it is not transmitted with the same efficiency throughout this range, and it has had very limited impacts on wild birds and livestock in the Neotropics despite evidence for widespread transmission.126,130,133,134 Canada represents the northern limit of WNV in the New World at 54 80 N; cases of human disease occur every year in southern Canada, particularly near Toronto, Montreal, and other cities of Ontario and Quebec, and in the prairie province of Saskatchewan, which has higher incidence but a smaller population. In 2009, the previously WNV-free area of British Columbia became the last of Canada’s southern tier of provinces to detect WNV activity, apparently enabled by above-average temperatures and high C. tarsalis mosquito abundance.135 There are two ways to think about northward viral expansion relevant for human health: shortterm climate variability may create local conditions for seasonal outbreaks of WNV, whereas longer-term trends may expand the range where sustained, endemic transmission is possible across years. How climate change might influence vector distributions and breeding seasons is an important consideration for public health officials,136 but WNV ecology is complex and varies geographically in respect to regional and seasonal variation in climate and environment and how these, in turn, impact population dynamics of the viral strains, vectors, amplifiers, and hosts. Models are helpful for broader predictions and 288
better understanding of which variables are drivers of change. However, inferring risk and vulnerability from models is challenging due to variation in spatial scales and modeling methods. The challenge to public health officials is to harmonize these data for local outbreak predictions and intervention planning.137
IS THE CIRCUMPOLAR NORTH VULNERABLE TO WNV? The rapidity and magnitude of warming in the Arctic is far greater than in other parts of the world—by some estimates, more than twice the global rate138,139 with some models predicting an increase in surface air temperature as high as 8 C over the next 100 years.140 Rapid changes to local weather and climate are challenging Arctic ecosystems’ resilience by rapid seasonal disruptions to both geophysical (e.g., permafrost freeze/thaw cycles, sea ice) and biological processes (e.g., reproduction).141 – 145 Climate models for the Arctic region present several scenarios that differ across regions and within local areas.146 Predictions for climate change in high latitude regions include an increase in annual mean precipitation, reductions in sea ice (with a mostly icefree Arctic Ocean in summers), reduction in nearsurface permafrost extent at higher Arctic latitudes by a minimum of 37% (multimodel average of 81%), and glacier volume reductions between 15–35%.147 Challenges include adaptations to higher temperatures, redistribution of species, extinction for those unable to adapt or shift ranges rapidly enough. Marine organisms in the polar regions are particularly vulnerable to overall increases in ocean acidity, reduced oxygen, and temperature extremes. Human populations residing in rural/remote areas (much of the Arctic), are particularly vulnerable to water availability/supply and food security. Population displacement has a greater impact on those communities that lack the resources for evacuation with permanent relocation.147,148 For example, the Alaskan coastal indigenous communities of Shishmaref, Kivalina, and Newtok are being displaced due to rising sea levels, land erosion, and/or permafrost thaw as a result of climate change; poor governmental response to climate change and relocation efforts (including allocating requisite funds) are having far-reaching impacts: lost sense of community and cultural practices, health impacts, and economic decline.149 For WNV to be transmitted consistently in the Arctic and sub-Arctic, it must adapt to narrower
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seasonal transmission windows and possibly new vectors and hosts.150 Temperatures in many areas of the Arctic between June and August regularly exceed the approximate WNV replication threshold of 14.3 C.20 Warming over the coming decades is likely to make the region slightly more receptive to WNV transmission, although sustained transmission will remain unlikely (Figure 2). Should WNV reach the circumpolar region, a number of competent host taxa are there already,151,152 especially during the summer breeding season when WNV transmission would be most likely to be sustainable. These summer-resident sub-Arctic birds include migrant American Robins that are key hosts of WNV at lower latitudes,36,153 several species of warblers that are highly competent for WNV,154 and possibly white-crowned sparrows that are highly competent for St. Louis encephalitis virus,155 which is very closely related to WNV. These long-distance migratory birds could provide a vehicle for introduction at far northern latitudes, and
there are also a number of other WNV-competent taxa30,39 represented in sub-Arctic summer populations, notably several species in family Corvidae (jays, crows, ravens, and magpies).151,156 In addition to temperature, another critical limitation for WNV’s expansion potential is that the vectors that maintain WNV in enzootic cycles are not found in the Arctic. For example, the Alaskan mosquito fauna is dominated by the genera Aedes and Culiseta,159 most of which feed primarily on mammals and therefore make very inefficient vectors for bird-borne WNV, even though related species in the continental United States have been moderately competent for transmitting WNV in laboratories and could serve as bridge vectors to humans.31 And, local transmission of avian malaria parasites has been detected in both resident and hatching-year migrant birds at 64 north latitude in the Fairbanks–Denali area of interior Alaska. It is unclear which mosquito species is transmitting the parasite, but it serves as
1950–2000
Risk level 1 (no risk) 2 3 4 5 2070 (RCP 4.5)
FI GU RE 2 | Suitability of July mean temperatures for WNV transmission in North America and Europe for 1950–2000 (upper panel) and as a multimodel mean for the moderate-warming representative concentration pathway 4.5 in 2070 from the IPCC’s 5th Assessment Report (lower panel). Transmission risk levels are assigned from 1 to 5 (blue to red) following threshold definitions in the California Mosquito-Borne Virus Surveillance and Response Plan157 based on experimental estimates of extrinsic incubation of WNV.20,158 Thresholds for risk correspond to the following temperatures: 1 (26.1 C). Both observed and future temperatures were obtained from WorldClim (http://worldclim.org), and future temperatures for RCP4.5 were averaged across the ensemble of available models.
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proof that mosquito-borne avian pathogens can be transmitted at such high latitudes.160 The short summers in the Arctic permit only 1–2 mosquito generations per year,159 which sharply limits the time available for viral amplification in bird-mosquito cycles, even though some univoltine (those producing one brood in a season) mosquitoes can be extremely abundant when they are active. If temperatures warm as expected and the climatic zones that presently support both key vector species and WNV transmission expand (Figure 3), marginal transmission at high latitudes may become possible over the next century. This would be more likely if vector expansion is aided by anthropogenic changes in land use that may accompany climate change, such as northward expansion of irrigated agriculture that could provide more consistent Culex habitat. A final consideration is human-environment interactions. Engagement with globalization is variable across populations and some populations still
engage in traditional subsistence economies, with sometimes the majority of goods derived from the local environment.166 Indigenous northern circumpolar populations engage in frequent environmental interactions that involve greater and prolonged direct contact with vectors (e.g., mosquitoes surrounding caribou herds) and birds (e.g. via hunting).167 Even with adequate land and climate data, models rarely account for human factors (e.g., land use, interactions with environment). Predictions of the impact of WNV transmission in currently endemic areas may not be accurate without consideration humanenvironment interaction data.
Circumpolar North Health Risk and Vulnerability Spanning 27 Arctic and sub-Arctic regions above 60 N, the northern circumpolar includes Alaska, parts of Canada, Norway, Sweden, Finland, parts of 1976–2000
Af Am As Aw BWk BWh BSk BSh Cfa Cfb Cfc Csa Csb Csc Cwa
2076–2100
Cwb CWc Dfa Dfb Dfc Dfd Dsa Dsb Dsc Dwa Dwb Dwc Dwd EF ET
F I G U R E 3 | Present and future climate classifications for North America and Europe based on the Koppen–Geiger system, which categorizes global climates based on annual patterns of temperature and precipitation. The top panel depicts classes for the observed period, 1976–2000,161,162 and the bottom panel represents multimodel mean climate under scenario B1 (similar to RCP4.5 in Figure 2) for 2076–2100 from the IPCC’s 4th Assessment Report.162,163 Published present-day northern limits for the key WNV vectors Culex pipiens and Culex tarsalis164,165 are shown for reference in red and blue across their respective geographic ranges. The range of C. pipiens spans most of the northern hemisphere, and C. tarsalis is limited to western North America. Note the northward expansion of Dfa and Dfb zones in North America (dark and medium purple), which are characterized by winter snows, year-round humidity, and warm or hot summers that currently support WNV transmission each year. Areas of Europe with hot summers (indicated by abbreviations ending in “a”: Cfa, Dfa, and Csa) also have had WNV disease cases annually and these areas are expected to expand with climate change.
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the Russian Federation, and island states (e.g., Greenland, Iceland, and Faroe Islands). The area is sparsely populated—roughly 10 million people across 17 million square kilometers, including the landmass of all territories and countries that overlap the circumpolar region.168 The proportion of indigenous to nonindigenous peoples varies among regions from ~90% in Greenland to
