The main environmental drivers, for change in vector-and rodent-borne diseases in circumpolar area.Written by Paula Williams 2010

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Arctic Fox


Background:

To understand vector- and rodent-borne disease changes we must first understand what is considered normal and stable conditions for arthropods and rodents in relation to the different biomes. To assume that the environment and ecosystems is a stable constant is to misunderstand diversity and dynamics of the ecology of varying viral lineage across temperate and boreal continents. For instance one of the key drivers of Hantavirus is the diversity of its rodent carriers and their robo carrying diseases are driven by masting. These northern rodents such as the bank vole, lemming and yellow necked mouse have varying susceptibility to a range of hantaviruses. Hantaviruses are worldwide emerging haemorrhagic fever viruses which are transmitted by the main reservoir of chronically infected rodents which contaminate humans by aerosolized excreta. The most prevalent Hantavirus in circumpolar area is Puumala Virus (PUUV) which causes nephropathia epidemica (NE). This condition is a form of haemorrhagic fever coupled with renal syndrome (HFRS). The importance of climate change is of importance when monitoring vector-rodent borne disease and changes in biota.


Introduction:

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I. ricinus
Virologists already understand about the differences and diversity in robo carrier rodents and the role of immuno-genetics. Therefore, within and among the rodent species the dynamics can considerably vary geographically. Similarly, with vectors (such as ticks eg I. ricinus) both regional climatic requirement variations and the existence of ‘demes’[[#_ftn1|[1]]a] have been demonstrated. This is also apparent amongst the Arvicoline rodent species where there is considerable variation between voles and lemmings susceptibility to tularemia.



Key environmental drivers:


There are many direct and indirect environmental drivers to vector-rodent-borne diseases. One of the key drivers for robo virus is dependent not so much on differential weathering patterns such as the impact of severe storms but rather on the seasonal patterns as to how the climate is changing the biota and the local ecology’s structure. Seasonality is a major factor that affects changes in rodent dynamics and their biodiversity. This driver can alter the robo carrier rodents impact of physical conditions on virus spreading capability. Rather, can affect incubation and hosting capabilities where change in seasonal patterns can be either an inhibitor or catalyst for spreading the disease to other hosts in future summer periods to human populations.
Likewise vector borne diseases are dependent on climate suitability. For example a tick population can be defined[[#_ftn2|[2]]1] as the fitness of a set of climatic conditions for the existence of that population in a given region. However, many other factors operating at different levels restrict the effective dispersal and establishment of potential invaders. Thus, while the climate in a particular location may be suitable for a given tick species, the potential for dispersal there and the ability to establish a new viable population may be very low. Therefore, with increase summer there is increase to human exposure and epidemic outbreak as virus rodents are ubiquitous. With the increase spring temperatures we get synergistic biological[[#_ftn3|[3]]2] and non biological factors which can add to high incidences to tick borne encephalitis (TBE). Thus, seasonal temperature anomalies are one of the key drivers to prevalence of the outbreaks to vector-rodent borne epidemics in human populations.


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Vole

Vole dynamics is another driver especially the impact on masting[[#_ftn4|[4]]3] in temperate and boreal forests or taiga. Thus, small changes in seasonality may affect the density dependent structure of the rodent dynamics and their biome related community structures. A high mast production in autumn means a higher food supply for them which allows for a higher survival rate. Masting increase in summer coupled with mild winter is a particularly important driver as the prediction of a potential ‘outbreak’ is likely to occur 2 years later for that summer. Such time-laps from voles in autumn ingesting the seeds and breeding is a process that can indicate human epidemic and hopefully be able to warn nearby dwelling and communities to be cautionary and or vaccinated for the prevention of disease for that predicted season. So indirectly deciduous forests are also drivers of robo viruses as tree seed population can be linked to outbreaks of rodent population the so called ‘vole years’. There is plenty of evidence[[#_ftn5|[5]]4] that can demonstrate that NE infections and mast years has a clear pattern to increase incidence of PUUV.

Other drivers that can alter the rodent dynamics are the climatic oscillation patterns such as El Nino and El Nina and the negative NAO bringing storms as opposed to the lesser storms from positive NAO. But as each biome is unique so are the related community dynamics .Particular predators and prey on rodents and arthropods in the snowy north can also affect the rodent and arthropod dynamics. The most common robo viruses in circumpolar area are Hantaviruses eg PUUV, Cowpox and Arenaviruses. There is lot of concern about high NE incidences in the north because of the typical northern environment conditions are rife for extended survival of rodent carriers and their potential transmission. Drivers such as low temperatures and high moisture are of importance for survival conditions for Puumala Virus (PUUV). Recently it has been found that PUUV may remain infectious for at least 2 weeks outside the host, up to 2 weeks in room temperature possibly much longer in cold temperatures and in moist conditions[[#_ftn6|[6]]5]

The key drivers for change in robo disease in circumpolar area is the direct climatic impacts on these viruses and hence geographic patterns that can lead to infection risk to human populations. The reasons for high NE incidence in Finland is due to the high forest coverage for forest rodents where the arvicolines and PUUV can then occur. Furthermore, in the northern taiga there are no barriers to inhibit the spread of the host and virus because the landscape is continuous and relatively homogenous for the bank vole and PUUV to survive. Ostensibly, PUUV spreads immediately from "survival pockets" to the whole landscape in the increase phase of the vole cycle. It is only in cyclic bank vole populations the number of susceptible bank voles reaches high enough abundance, and high number of freshly infected voles, resulting in high viral load in the environment.

There appears to be a misunderstanding[[#_ftn7|[7]]6] however, about warmer winters resulting in a Hanta outbreak the following summer? It is not the warming winters that are the driver of Hanta for the following summer as rodent peak does not result in 2-3 months, it is a result of a longer term processes. This can be from 2 -3 years from when masting increases the food supply to voles in autumn, then incubation in winter to the following summer where vectors feed on the rodent infected virus and the vector larvae then complete their cycle as co feeders in the vector as mechanical hosts where transmission of virus without the host being viremic can increase its viral transmission geographically beyond the biota to other biomes and hence greater threats to human populations.


As an example: [[#_ftn8|[8]]7] If NE peaks in year 0 are induced by abundant mast formation say in year-1, thus facilitating bank vole survival during winter, this then puts the local human population at risk from the spring onwards of year 0. Therefore, this bank vole survival could be further promoted by higher autumn temperatures in year-1, whereas mast formation itself is primed by higher summer temperatures in year-2. It has been noted lately by Clement et al (2009) that both summer and autumn temperatures have been rising to significantly higher levels during recent years. This therefore would explain the almost continuous epidemic state since 2005 of a zoonosis, which up until recently was considered rare in the North. Moreover, in 2007 a NE peak and an abundant mast formation occurred for the first time within the same year, thus forecasting yet another record NE incidence for 2008. Scientists therefore can predict that with the anticipated climate changes due to global warming, NE might become a highly endemic disease in Belgium and surrounding countries such as the circumpolar area.

Ideally, the viruses survive better in cold, not in warm environments so the rodents whilst they may survive better in a mild winter and breed earlier after a warm winter warming is interrelated to the survival of voles and hence, affect the distribution of carrier species and their pathogens, and dynamics of carrier species. Mainly the increase variability in winter climate, warm spells and consequent freezing events will force rodents to look for new shelter and immigrate to human settlements. Warming as an environmental driver can increase the voles breeding capacity because of the length of the breeding season and because there is less snow to enhance winter survival. Conversely, they succumb to be less protected with less snow as prey for local predators which can indirectly decrease their survival and increase their predators survival.

Another driver of environmental change is related to agriculture and fauna[[#_ftn9|[9]]8]. Over the years we can see the changes in the use of the former agricultural land. There are fields overgrown now with much older trees which have the capacity to produce more masting in temperate zones. The forest provide greater timber usage for fuel and industry which enhances risk and carrier rodent species to immigrate into woodsheds in autumn in nearby human settlements. Reindeer husbandry in the north and bushy habitats also provides ecologically new habitats for vectors like ticks to feed on forest dwelling virus carrying species like arvicolines to move closer towards human settlements and communities. The likelihood for human incidence of infection is increased with travelling and hiking through forests especially with ticks. Birds are equal drivers and contributors for transmission and spread of robo and vector borne diseases. Mid-March and early April are the main periods of mass arrival of birds in Spain on their way to northern Europe Interestingly, certain migratory birds are carriers of immature hyalomma ticks in the circumpolar area and have the potential to introduce them into currently hyalomma-free areas in the spring. However, studies do not suggest that they can become established based on their recent climate requirements and current climate data.

Arthropods are of great importance as transmitters of disease-producing agents to man and other animals. Disease transmission can be accomplished in two ways. One way is mechanical where the arthropod eg tick carries an infectious organism such as Lyme’s disease from one person or object to the next without being a host for the development of the organism. The second way is transmission where the arthropod becomes the intermediate host for the infection to multiply within the host and then transmitted to vertebrate host. The infections that require an arthropod host for completion of their life cycle use their hosts as vectors to produce vector borne diseases in vertebrate such as human populations. However, when we get rodent and vector as intermediate hosts then the proliferation of the disease to human population becomes an epidemiological concern eg. tick born diseases (TBD).

TBEV life cycle rely heavily on previous autumn temperatures for the establishment of permanent tick populations. For example the H. marginatum a viral zoonosis tick responsible for Crimean-Congo hemorrhagic fever (CCHF) requires temperature that have a cumulative average of 800°C in to maintain permanent populations, where below 400°C they cannot be colonized as it affects molting of immature stages in these sites.[[#_ftn10|[10]]9] Temperatures are drivers that can strongly influence tick activity patterns. For example there was an unusually mild winter of 2006/7 was in eastern Germany[[#_ftn11|[11]]10] where there was a significant outbreak of TBE. This anomaly of normal cold season demonstrates the effects of TBE and specificity to temperature dependency. Because viral infectivity for ticks lasts only a few days in rodents, larval and nymphal ticks must feed synchronously on rodents to permit persistent transmission cycles. This is associated, both statistically and biologically, with a relatively rapid rise in temperatures during spring so that the threshold for larval activity (c.10°C weekly mean max temp) follows very soon after the threshold for nymphal activity (c.7°C). This factor may be exploited for risk assessment (Randolph et al. 1999).

The transmission of TBE and dynamics of vertebrate hosts due to climate change are mainly from voles which are excellent hosts for tick borne encephalitis and other tick borne pathogens. Other co-feeding intermediary hosts are Roe deer as well as wild boar can also be a good host for ticks especially I. ricinus in Sweden during warmer climates. The larvae and nymphs in relation to mouse density is important driver for proliferation of TBE. So the drivers can be classified as ‘cause and effect’ when it comes to understanding the reasons for emergent vector-rodent borne diseases in circumpolar north. Whereby, climate causes the effects on masting, hence, masting causes effects on the rodents, and therefore, the rodents cause effects on the larvae, whereby the larvae causes effects on the nymphs, and thus time lag causes an effect of 2- 3 years for the prevalence of a potential human epidemic. There is of course the so called ’Dilution effect’ where high diversity of incompetent hosts can "dilute" the tick load and reduce the virus pressure/commonness. This is in contrast of course with climate change on the biodiversity for the abundance of infected ticks. Lyme disease is spread very efficiently by the drivers of fallow deer with incidence increases particularly after mild winters and during warm humid summers. The human infection is mostly from nymphal ticks than adults. However, though the increase of competent hosts (wood mouse, bank vole) stimulates Lyme borreliosis (LB) incidence (transmitted by I. persulcatus,) risk increases with deer, wild boar and grouse densities as important key drivers of the disease.

Direct and indirect drivers of vector born disease in Circumpolar North

00010033.jpgIt has been observed that direct drivers such as mild winters and warm summers will increase lyme disease. The factors triggering TB disease change, in addition to climate change according to Süss et al. 2008 there are also indirect environmental drivers which suggest that more use of the environment can leads to higher exposure. For example affluent countries, inhabitants have more leisure time, retired people are healthy and active, and they collect mushrooms, berries, and also firewood. In low socioeconomic countries unemployment is a great problem and inhabitants collect firewood, mushrooms, and berries to improve their economic conditions. The other factors is change in farming which leads to higher exposure. This also can include farm holidays (drinking of unpasteurized milk might cause alimentary TBE), agricultural land set aside because of EU subsidies leads to fallow, and scrublands that in turn increase the number of hosts for ticks.

We must not forget also the primary and preventative measure for immunization. It is apparent that the rate of vaccination against TBE is minimal across most countries in the circumpolar area .which gives rise to TBE risk, especially too as travelers are not sufficiently informed about the risks in those areas. Although changes in climate and the length of different seasons will directly affect tick survival, activity, and development, there is no real evidence that rising temperatures will result in a greater abundance of ticks by simply increasing rates of development. Rather it is observed that changes in development rates could make tick cohorts available to different diapause windows (largely determined by day length)[[#_ftn12|[12]]11], thus changing patterns of seasonal activity. Indirect effects of climate change will impact the number of infected ticks by affecting vegetation. For example, a warming climate in central Europe is likely to result in a decrease of Norway spruce (Picea abies) and the areas involved will probably be colonized by beech (Fagus sylvatica)[[#_ftn13|[13]]12] the fallen leaves of which provide a favorable microclimate for survival of the free-living tick stages ( not to mention the increase masting impact for the attraction of voles). Additionally, climate change will also have indirect effects on tick-borne pathogen transmission by affecting the survival and abundance of tick maintenance hosts, such as deer, and pathogen-reservoir hosts such as rodents and birds. Climate change may also influence disease risk by affecting the long-term use of land (e.g, farming, tourism, etc.), and weather patterns have an effect by influencing short-term human behavior such as picnics and mushroom picking. Climate effects are more easily noticeable close to the geographical distribution limits of both vector and disease. The magnitude of the effects of climate change in an endemic area depends on local conditions and vulnerability, and is determined not only by ecological conditions but may be influenced by socioeconomic factors, human migration and settlement, ecosystems and biodiversity, migrating patterns of birds, land-use and land cover changes, human cultural and behavioral patterns, and immunity in the population. Since some of these conditions are in turn influenced by climate change, a complex chain of processes exists that makes the precise factors responsible for changes in disease incidence often difficult to determine.

Vector-borne diseases (VBD) are infections transmitted by the bite of infected arthropod species, such as mosquitoes, ticks, triatomine bugs, sandflies and blackflies. Mosquitoes, which can carry many diseases, are very sensitive to temperature changes. Warming of their environment within their viable range has the ability to boost their rates of reproduction and hence, the number of blood meals they take. This then prolongs their breeding season, and shortens the maturation period for the microbes they disperse. Mosquitoes and the diseases they carry including malaria, dengue fever, Ross River virus, and West Nile virus are especially sensitive to temperature changes and land elevation. Rates of insect biting and the maturation of microorganisms within them are temperature-dependent, and both rates increase when the air warms, enhancing the chances for disease transmission. In highland regions, as permafrost thaws and glaciers retreat, mosquitoes and plant communities are migrating to higher ground. These climate warming for vector disease carriers is a grave concern to circumpolar north.


Summary:

Climate change and infectious diseases, from World Health Organization describes how diverse environmental changes are key drivers that affect the occurrence of various infectious diseases in humans. These include dams, canals, irrigation which can be literally reservoirs for malaria, schistosomiasis, helminthiasis from vector intermediate hosts such as snails, mosquitoes and larval contact to moist soil. Agricultural intensification can cause drivers such as increase rodent abundance and vector resistant insecticide species on crops and forests. Urbanization and crowding from transient populations from climate affected area can succumb to cholera from poor sanitation and rodent borne infected catchments such as cholera outbreak after earthquake, tsunamis and severe storms and flooding. This then could lend into deforestation and new habitation which could increase vector borne sites such as malaria also reforestation can lead to lyme disease from tick hosts and outdoor exposure. The effects of ocean warming giving rise to red tide disease from toxic algal blooms. Not to mention elevated precipitation which has the ability to provide rodent dynamics breeding grounds because of food and habitat abundance for spread of hantavirus, and breeding pools for mosquitoes for spreading rift valley diseases. Thus, soil moisture is another driver in the virus ecology especially for PUUV. Importantly, by investigating PUUV data from each season, studies can monitor a number of significant relationships and drivers between cases of NE and climate. For example, outbreaks of NE appear to be influenced by drivers such as a cold and moist summer three years previously causing growth of trees and abundant mast two years later. Drivers also ca be a hot summer two years previously causing stimulation of bud formation and abundant mast one year later. Another influential driver is a warm autumn one year previously promoting the survival of bank voles.

Conclusion:


The Intergovernmental Panel on Climate Change (IPCC)[[#_ftn14|[14]]13] projections of increased temperature and precipitation suggest that there is definitely an emergence of more disease-friendly conditions in regions that did not previously host diseases or disease carriers. Climate change is a key driver which has the ability to accelerate the spread of disease primarily because warmer global temperatures enlarge the geographic range in which disease-carrying animals, insects and microorganisms as well as the germs and viruses they carry can survive. In addition to changing weather patterns, climatic conditions affect diseases transmitted via vectors such as mosquitoes (vector-borne disease) or through rodents (rodent-borne disease). The predictive power of simple environmental and climate drivers can be useful for health authorities to predict and therefore adjust their primary and preventative care policies for Circumpolar area against the potential harmful effects of the emergent vector-rodent-borne disease to human populations in the future.

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Supporting Web sites

http://www.isw-tbe.info
(//http://www.dwd.de//, data from Potsdam)
http://www.zecken.at/zecken.aspx
http://www.tbefacts.com
http://www.szu.cz/cem/klistata/klistata.htm


[[#_ftnref1|[1]]a] (defined as populations of closely related interbreeding organisms of the same species with differing responses to the wide array of climate factors occurring across the geographical range of the species).
[[#_ftnref2|[2]]1] J. S. Gray et al Effects of Climate Change on ticks and TBD in Europe
[[#_ftnref3|[3]]2] Lancelot, R and Hendrickx, G
[[#_ftnref4|[4]]3] (seeds of deciduous broad leaf trees eg. acorns)
[[#_ftnref5|[5]]4] Tersago K (2008)-NE in Belgium
[[#_ftnref6|[6]]5] Kallio et al.2006-,(J Gen Virol)
[[#_ftnref7|[7]]6] Henttonen,H (2009) optima vodcast MCH semeste2 vector- and rodent –borne disease
[[#_ftnref8|[8]]7] 3 Jan Clement et al; 2009. Epidemiology, Scientific Institute for Public Health, Juliette Wytsmanstraat, Belgium
[[#_ftnref9|[9]]8] Bradley MJ
[[#_ftnref10|[10]]9] Dautel and Hoogstraal
[[#_ftnref11|[11]]10] (//http://www.dwd.de//, data from Potsdam)
[[#_ftnref12|[12]]11] Gray, JS
[[#_ftnref13|[13]]12] Kölling C. Forests under the influence of climate change
[[#_ftnref14|[14]]13] IPCC- An Assessment of the Intergovernmental Panel on Climate Change