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Virulent pathogen

FIGURE 2-19 The plant disease triangle, illustrating the relationship between host, pathogen, and environment necessary for disease to occur.

Conducive environment

FIGURE 2-19 The plant disease triangle, illustrating the relationship between host, pathogen, and environment necessary for disease to occur.

individuals encounter mates. For example, the Karnal bunt pathogen requires encounters between two mating types for reproduction to occur, yet its propa-gules are wind dispersed, making encounters between individuals of different mating types unlikely when populations are small. The resulting Allee effect may help to explain why this species has not been more invasive, since encounters between mating types will be even less likely when dispersed by wind over larger areas (Garrett and Bowden, 2002). For species that experience them, such Allee effects interact with disease nonconducive environmental conditions to reduce the chance of infection still further. As a result, if climatic conditions become more conducive to disease so that pathogens are released from the constraint of the Allee effect, pathogen populations may increase much more rapidly than anticipated.

The typical "compound interest" development of plant disease epidemics for pathogens with multiple generations per season can also result in important threshold structures. Infection levels can often increase by orders of magnitude toward the end of the season. If the length of the growing season increases, regional production of particular crop species may expand over time, with the longer season length allowing for huge increases in pathogen populations toward the end of the growing season. These populations may reduce yields during that season and also serve as large sources of inoculum for upcoming cropping seasons. Such higher regional inoculum loads may produce positive feedback loops, rendering local application of some management techniques less useful. For example, local application of techniques such as sanitation (removal of infected plant materials), use of cultivar mixtures, and use of disease resistance based on lower inoculum production all rely, at least to some extent, on an ability to control

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local inoculum loads. If regional inoculum loads are too high, the contributions of these methods will be diminished (Garrett et al., in revision). Likewise, in wildland systems, plant diversity probably provides baseline regulation of plant disease that is unappreciated but may be diminished if systems become saturated with inoculum. Conversely, if seasons become shorter or if climatic conditions during significant parts of growing seasons become less disease conducive, greater benefits may be obtained from some management techniques.

Pathogen range shifts may occur as climatic conditions change to allow infection and overwintering or oversummering in new areas. The effects of climatic shifts may interact with other phenomena, such as the introduction of new pathogen species or pathogen genotypes. For example, overwintering of the potato late blight pathogen is facilitated by the presence of different mating types, which allows sexual production of a much hardier oospore and the potential for adaptation through production of new genotypes (Widmark et al., 2007). The combination of milder winters and introduction of new mating types may greatly increase problems with such pathogens. Range shifts and pathogen introductions will also result in new encounters between pathogen species, with the potential for hybridization to produce new pathogens (Brasier, 2001). Likewise, the introduction or range shift of new vector species may make diseases much more important, such as in the case of the movement of the glassy-winged sharpshooter and resulting increased risk of Pierce's disease of grapevines (Redak et al., 2004).

Phenological shifts and range shifts in response to climate change may not follow the same patterns for plant hosts and pathogens. Some pathogens can only infect particular plant growth stages or organs, such as flowers. For example, the Fusarium head blight pathogen infects wheat anthers or other floral organs (Bai and Shaner, 2004). Shifts in flowering time phenology in response to climate change may not match shifts in pathogen phenology such that infection rates may unexpectedly rise or fall. Different patterns of geographic range shifts may result in new pathogen-host combinations (Parker and Gilbert, 2004). The genetic potential for adaptability of pathogen populations will be important in determining whether any resulting reductions in infection will be short term or lasting. In general, the timeline of pathogen adaptation is likely to be much shorter than the timeline for plant adaptation. This will be especially true for long-lived plant species in wildlands, but also for annual crop species even with the full attention of agricultural scientists.

Policy may also interact in important ways with abiotic conditions. Along with the Irish potato famine, another dramatic example is the dustbowl in the central United States. Policies that supported extensive plowing of lands in this area coincided with climatic conditions favoring wind erosion of soils. Either factor alone might have caused problems, but the combination of the two led to conditions devastating to the region. The interaction of biological and sociological factors may also result in amplified effects of climate change. For example, if

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plant pathogens are intentionally introduced (Fletcher and Stack, 2007; Madden and Wheelis, 2003), bioterrorists using them might seek out the most environmentally conducive conditions for their establishment in vulnerable cropping systems. Regions where local food security is closely tied to local food production will be particularly vulnerable to changes in crop disease pressure. Yet societies in these regions may also tend to rely on crop species that are less well supported by research and development. These "orphan crops," such as millet, quinoa, cassava, and teff, need more research support to buffer the vulnerability of societies to which they are important (Nelson et al., 2004).

Responding to Climate Change

The good news for formulation of strategies for plant disease management under changing climate conditions is that much of what needs to be done is the same with or without climate change. Even if there were no long-term trend in climatic parameters, climatic variation from season to season, year to year, and region to region requires knowledge and tools for adapting to the different scenarios. However, the potential for new combinations of climatic variables, along with the potential for interactions and for more rapid variation in conditions, reinforces the need for research and policy responses to plant disease risk (Coakley et al., 1999; Garrett et al., 2006). Research directed explicitly toward understanding the complexity of system responses to climate change is needed.

A mechanistic understanding of plant and pathogen responses to climate change will be based on characterizing current populations and their potential for adaptation. New genomic tools make it possible to characterize gene expression and genotypic diversity much more readily in both wildland and agricultural plant communities. These tools can be applied in concert with other "-omics" approaches to link responses in gene expression (transcriptomics), lipidomics, and metabolomics for a fuller mechanistic understanding of adaptive potential. These approaches will have to be applied in multifactor studies of climate change effects, so that the interactions between the effects of changes in temperature, precipitation, CO2, and other environmental factors can be understood, along with the potential for adaptation.

Tools for the study of pathogen population and community structure, gene expression, and other responses are evolving rapidly. Advances in sequencing technologies make the routine characterization of microbial communities feasible (Riesenfeld et al., 2004; Roesch et al., 2007) and will eventually make it inexpensive. Microarrays, such as the GeoChip (He et al., 2007), are being designed to study microbial gene function in soils. New microarrays are needed to study the presence and expression of microbial genes related to plant disease. It will be important to collect baseline information about microbial community structure and function soon, so that changes in microbial communities under new climatic conditions can be studied. Experiments to compare responses of microbial com-

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munities to new environments will also be important (e.g., Waldrop and Firestone, 2006). Undoubtedly there are many forms of disease suppressiveness provided by microbial communities in soils that offer benefits to agriculture and regulate disease in natural systems and are currently underappreciated.

Research to clarify the effects of host landscape structures will help to improve strategies and will be necessary for studying changes at regional, continental, and global scales. Current regional analyses of climatic effects on disease risk tend to be calculated for disease risk in individual "pixels," important for developing a first-approximation estimate of risk. The next stage for such models will be to incorporate risk neighborhoods to improve estimates, where the risk for any given location will increase with proximity to higher-risk areas. Finally, regional and global models will need to incorporate pathogen evolution. Formulating and parameterizing these models will require advances in epidemiological theory and experimentation. For example, better data and models related to pathogen and host dispersal, current levels of intraspecific diversity, and the strength of selection under different climate change scenarios are needed.

Long-term geographically representative records of disease occurrence and the distribution of pathogens and hosts are rare, despite their importance for understanding epidemiology and trends in epidemics (Jeger and Pautasso, 2008). Global networks supporting the analysis of epidemics are needed. Progress toward this goal is in place; for example, the United States has developed a National Plant Diagnostic Network to facilitate data collection and analysis (Stack and Fletcher, 2007). To be most effective, this network ultimately needs to be linked with comparable national networks in other countries. It is to the advantage of the United States to assist other countries in setting up such networks for gathering and analyzing data, so that we can all benefit from more complete information. The use of model predictions for modifying agricultural management has proven useful in many parts of the world, including applications by resource-poor farmers based on climate predictions in Zimbabwe (Patt et al., 2005).

One of the most important investments we can make is in conservation, characterization, and the development of strategies for optimal use of plant genetic resources. In wildland systems, conservation is necessary to increase the chances that plant populations are large enough to include individual genotypes adapted to new climate scenarios. In agricultural systems, conservation of diversity in crop species and their wild relatives is necessary to increase the chances that genes needed for resistance and tolerance to new biotic and abiotic stresses are maintained (Johnson, 2008). In situ conservation allows natural selection to continue acting on these species. Ex situ conservation is a useful backup strategy and simplifies some analyses of accessions. International networks for conservation of crop genetic diversity, such as the institutions in the Consultative Group for International Agricultural Research (CGIAR), are critical for ensuring conservation and analysis of accessions. The funding currently available for such programs is very low compared to the importance of their mission. While investments such

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as the Svalbard Global Seed Vault provide a last resort, active investigation of plant resources is needed.

Ultimately our best response to the challenge of climate change in agriculture will be to develop diverse, flexible, and resilient agricultural systems that can adapt more readily to new climatic conditions. These systems will have to include well-prepared and well-funded agricultural scientists working globally to develop new strategies. In wildland systems, replacing plant species or genotypes at risk is a less attractive option. Since invasive pathogens can have the most important effects and have the potential to exacerbate the effects of climate change, policies to better reduce the spread of exotic pathogens will be important (Anderson et al., 2004; Burdon et al., 2006).

Acknowledgments

I appreciate valuable comments from members and staff of the Forum on Microbial Threats, R. Bowden, D. Rotenberg, and P. Garfinkel. It is also a pleasure to acknowledge support by the U.S. National Science Foundation (NSF) through Grant DEB-0516046 and NSF Grant EF-0525712 as part of the joint NSF-National Institutes of Health (NIH) Ecology of Infectious Disease program; by the U.S. Agency for International Development (USAID) to the Office of International Research, Education, and Development (OIRED) at Virginia Tech for the Sustainable Agriculture and Natural Resource Management (SANREM) Collaborative Research Support Program (CRSP) under Award No. EPP-A-00-04-00013-00 and for the Integrated Pest Management (IPM) CRSP under Award No. EPP-A-00-04-00016-00; and by the Kansas State Experiment Station (Contribution No. 08-308-B).

CLIMATE CHANGE AND INFECTIOUS DISEASE: IMPACT ON HUMAN POPULATIONS IN THE ARCTIC12

Alan J. Parkinson, Ph.D.13 Centers for Disease Control and Prevention

Introduction: The Arctic Environment

The circumpolar region is defined as the region that extends above 60oN latitude, borders the Arctic Ocean, and includes all of or the northern parts of eight nations: the United States (Alaska), Canada, Greenland, Iceland, Norway,

12The findings and conclusions in this report are those of the author and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

13Arctic Investigations Program, Division of Emerging Infections and Surveillance Services, National Center for Preparedness Detection and Control of Infectious Disease, Anchorage, AK.

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Finland, Sweden, and the Russian Federation (see Figure 2-20). The climate in the Arctic varies geographically from severe cold in arid uninhabited regions to temperate forests bordering coastal agrarian regions. Approximately 4 million people live in the Arctic and almost half reside in northern regions of the Russian Federation. Peoples of the Arctic and sub-Arctic regions live in social and physical environments that differ substantially from those of their more southern dwelling counterparts. These populations are comprised of varying proportions of indigenous and nonindigenous peoples (Stephansson Arctic Institute, 2004; see Figure 2-21).

The indigenous populations of northern Canada (Northwest Territories, Yukon, Nunavut, northern Quebec, and Labrador), Alaska, and Greenland generally reside in small communities in remote regions. They have little economic infrastructure and depend on subsistence hunting, fishing, and gathering of food for a significant proportion of their diet. In these remote areas, access to public health and acute care systems is often marginal and poorly supported. Life expectancy of the indigenous peoples of Alaska, northern Canada, and Greenland is lower than that of the general populations of the United States, Canada, and Nordic countries (Young, 2008). Similarly the infant morality rate for the indigenous segments of these populations is higher than that of the comparable national populations. Mortality rates for heart disease and cancer, once much lower among the indigenous populations of the United States, Canada, and northern European countries, are now similar to their respective national rates. The indigenous populations of Alaska, Canada, and Greenland have higher mortality rates for unintentional injury and suicide. Other health concerns of the indigenous peoples of the Arctic include the high prevalence of certain infectious diseases, such as hepatitis B, Helicobacter pylori, respiratory syncytial virus (RSV) infections in infants, and sexually transmitted diseases, as well as heath impacts associated with exposures to environmental pollutants, rapid economic change and modernization, and climate change (Bjerregaard et al., 2004).

Climate Change and the Arctic Environment

The Arctic, like most other parts of the world, warmed substantially over the twentieth century, principally in recent decades. Arctic climate models project continued warming with a 3-5oC mean increase by 2100. The winters will warm more than summers, the mean annual precipitation is projected to increase, and continued melting of land and sea ice is expected to increase river discharge and contribute to rising sea levels. These changes will be accompanied by greater overall climate variability and an increase in extreme weather events (Arctic Council, 2005).

The rapid warming in the Arctic is already bringing about substantial ecological and socioeconomic impacts, many of which result from the thawing of permafrost, flooding, and shoreline erosion resulting from storm surges and

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FIGURE 2-20 The circumpolar region showing administrative jurisdictions. SOURCE: Map by W. K. Dallmann. Reprinted from Young (2008) with permission from W. K. Dallmann and the International Journal of Circumpolar Health. Copyright 2008.

loss of protective sea ice. In many communities, the built infrastructure is supported by permafrost. Loss of this permafrost foundation will result in damage to water intake systems and pipes, and may result in contamination of the community water supply. In addition, loss of foundation support for access roads, boardwalks, water storage tanks, and wastewater treatment facilities will render water distribution and wastewater treatment systems inoperable. Several villages already face relocation because village housing, water system, and infrastructure are being undermined (Warren et al., 2005).

Rapid warming has resulted in the loss of annual Arctic sea ice. On September 11, 2007, the Arctic sea ice cover reached the lowest extent recorded since

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FIGURE 2-21 The circumpolar region showing indigenous and nonindigenous population distributions.

SOURCE: Reprinted from Stefansson Arctic Institute (2004) with permission from W. K. Dallmann, Norwegian Polar Institute and the Stefansson Arctic Institute. Copyright 2004.

FIGURE 2-21 The circumpolar region showing indigenous and nonindigenous population distributions.

SOURCE: Reprinted from Stefansson Arctic Institute (2004) with permission from W. K. Dallmann, Norwegian Polar Institute and the Stefansson Arctic Institute. Copyright 2004.

observations began in the 1970s, exceeding the most pessimistic model predictions of an ice-free Arctic by 2050 (Richter-Menge et al., 2008; Figure 2-22). This dramatic reduction in sea ice will have widespread effects on marine ecosystems, coastal climate, human settlements, and subsistence activities. For the first time the reduction in annual sea ice has created ice-free shipping lanes to the northwest, from northern Labrador through the Arctic archipelago in northern Canada, to the Bering Strait, and has almost completely cleared a passage to the northeast, from the Bering Strait along the northern coast of the Russian Federation to Norway (see Figure 2-23). Both routes represent time- and fuel-saving shortcuts between the Pacific and Atlantic Oceans and will bring an increase in marine transport and access to vast oil, gas, and mineral reserves once inaccessible to exploration and exploitation.

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FIGURE 2-22 The Arctic ice cap, September 2001 (Top) and September 2007 (Bottom).

SOURCE: NASA, as printed in Borgerson (2008).

FIGURE 2-22 The Arctic ice cap, September 2001 (Top) and September 2007 (Bottom).

SOURCE: NASA, as printed in Borgerson (2008).

Such access will bring many benefits as well as risks to once isolated Arctic communities. Construction of new coast guard or military bases and other industrial ventures will bring employment opportunities to local populations, but will also affect population distribution, dynamics, culture, and local environments. Tourism will most likely increase. Public sector and government services will then increase to support the new emerging economies. These events will greatly

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FIGURE 2-23 Proposed northwest and northeast shipping lanes through the Arctic Ocean joining the Atlantic and Pacific Oceans.

SOURCE: Map by C. Grabhorn Reprinted from ACIA (2004) with permission from Cambridge University Press and C. Grabhorn.

FIGURE 2-23 Proposed northwest and northeast shipping lanes through the Arctic Ocean joining the Atlantic and Pacific Oceans.

SOURCE: Map by C. Grabhorn Reprinted from ACIA (2004) with permission from Cambridge University Press and C. Grabhorn.

challenge the traditional subsistence way of life for many communities and lead to rapid and long-term cultural change, which will create additional stress on an already vulnerable population (Curtis et al., 2005).

Climate Change and Human Health

The direct health effects of climate change will result from changes in ambient temperature, altered patterns of risk from outdoor activities, and changes in the incidence of infectious diseases. As ambient temperature increases, the

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incidence of hypothermia and associated morbidity and mortality may decrease. Conversely hyperthermia may increase, particularly among the very young and the elderly (Nayha, 2005). However, because of the low mean temperature in many Arctic regions, the likelihood of such events having large impacts on public health for the general population is low. More significantly, unintentional injury, mostly related to subsistence hunting and fishing—already a significant cause of mortality among Arctic residents—may increase (Arctic Council, 2005). The reduction in river and sea ice thickness, curtailed ice season, reduced snow cover, and permafrost thawing will make hunting and gathering more difficult, dangerous, and less successful, thereby increasing the risk of injuries and death by drowning.

Permafrost thawing erosion or flooding can force relocation. Communities and families undergoing relocation will have to adapt to new ways of living, may face unemployment, and will have to integrate and create new social bonds. Relocation may also lead to rapid and long-term cultural change and loss of traditional culture, which will increase individual and community stress, leading to mental and behavioral health challenges (Hess et al., in press).

Climate change already poses a serious threat to the food security of many Arctic communities because of their reliance on traditional subsistence hunting and fishing for survival. Populations of marine and land mammals, fish, and waterfowl may be reduced or displaced by changing habitats and migration patterns, further reducing the traditional food supply. Release of environmental contaminants from the atmosphere and melting glaciers and sea ice may increase the levels of these pollutants entering the food chain, making traditional foods less desirable (AMAP, 2003). Reduction in traditional food supply will force indigenous communities to depend increasingly on nontraditional and often less healthy Western foods. This will most likely result in increasing rates of modern diseases associated with processed foods, such as obesity, diabetes, cardiovascular diseases, and outbreaks of food-borne infectious diseases associated with imported fresh and processed foods (Bjerregaard et al., 2004; Orr et al., 1994).

Many host-parasite systems are particularly sensitive to climate change. Specific stages of the life cycles of many helminths may be greatly affected by temperature. For example, small increases in temperature can substantially increase the transmission of lung worms and muscle worms pathogenic to wildlife that are important as a food source for many northern communities (Hoberg et al., 2008).

Climate Change and Infectious Diseases in the Arctic

It is well known that climate and weather affect the distribution and risk of many vector-borne diseases, such as malaria, RVF, plague, and dengue fever in tropical regions of the globe. Weather also affects the distribution of food- and water-borne diseases and emerging infectious diseases, such as West Nile virus,

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hantavirus, and Ebola hemorrhagic fever (Haines et al., 2006). Less is known about the impact of climate change and the risk and distribution of infectious diseases in Arctic regions. It is known that Arctic populations have a long history of both endemic and epidemic infectious diseases (Parkinson et al., 2008). However, with the introduction of antimicrobial drugs, vaccines, and public health systems, morbidity and mortality due to infectious diseases have been greatly reduced. Despite these advances, high rates of invasive diseases caused by Streptococcus pneumoniae, Haemophilus influenzae, and Mycobacterium tuberculosis persist (Bruce et al., 2008a,b; Christensen et al., 2004; Dawar et al., 2002; Degani et al., 2008; Gessner et al., 1998; Meyer et al., 2008; Netesov and Conrad, 2001; Nguyen et al., 2003; Singleton et al., 2006; S0borg et al., 2001). Sharp seasonal epidemics of viral respiratory infections also commonly occur (Bulkow et al., 2002; Karron et al., 1999; Van Caeseele et al., 2001). The overuse of antimicrobial drugs in some regions has led to the emergence of multidrug-resistant S. pneumoniae, Helicobacter pylori, and methicillin-resistant Staphylococcus aureus (Baggett et al., 2003, 2004; McMahon et al., 2007; Rudolph et al., 1999, 2000).

The impact of climate on the incidence of these existing infectious disease challenges is unknown. In many Arctic regions, however, inadequate housing and sanitation are already important determinants of infectious disease transmission. The cold northern climate keeps people indoors amplifying the effects of household crowding, smoking, and inadequate ventilation. Crowded living conditions increase person-to-person spread of infectious diseases and favor the transmission of respiratory and gastrointestinal diseases and skin infections. Many homes in communities across the Arctic lack basic sanitation services (e.g., flush toilet, shower or bath, kitchen sink). Providing these services is difficult in remote villages where small isolated populations live in a harsh cold climate. A recent study in western Alaska demonstrated two to four times higher hospitalization rates among children less than 3 years of age for pneumonia, influenza, and childhood RSV infections in villages where the majority of homes had no in-house piped water, compared with villages where the majority of homes had in-house piped water service. Likewise, outpatient Staphylococcus aureus infections and hospitalization for skin infections among persons of all ages were higher in villages with no in-house piped water service compared to villages without water service (Hennessy et al., 2008). Damage to the sanitation infrastructure by melting permafrost or flooding may therefore result in increased rates of hospitalization among children for respiratory infections, as well as an increased rate of skin infections and diarrheal diseases caused by bacterial, viral, and parasitic pathogens.

Some infectious diseases are unique to the Arctic and lifestyles of the indigenous populations and may increase in a warming Arctic. For example, many Arctic residents depend on subsistence hunting, fishing, and gathering for food, and on a predictable climate for food storage. Food storage methods often include above ground air-drying of fish and meat at ambient temperature, below ground

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cold storage on or near the permafrost, and fermentation. Changes in climate may prevent the drying of fish or meat, resulting in spoilage. Similarly, loss of the permafrost may result in spoilage of food stored below ground. Outbreaks of food-borne botulism occur sporadically in communities in the United States, Canadian Arctic, and Greenland and are caused by ingestion of improperly prepared fermented traditional foods (CDC, 2001; Proulx et al., 1997; Sobel et al., 2004; S0rensen et al., 1993; Wainwright et al., 1988). Because germination of Clostridium botulinum spores and toxin production will occur at temperatures greater than 4°C, it is possible that warmer ambient temperatures associated with climate change may result in an increased rate of food-borne botulism in these regions. Preliminary studies have shown that fermentation of aged seal meat challenged with C. botulinum at temperatures above 4oC results in toxin production (Leclair et al., 2004).

Outbreaks of gastroenteritis caused by Vibrio parahaemolyticus have been related to the consumption of raw or inadequately cooked shellfish collected from seawater at temperatures of higher than 15oC. Prior to 2004, the most northerly outbreak occurred in northern British Columbia in 1997. However, in July 2004, an outbreak of gastroenteritis caused by V. parahaemolyticus was documented among cruise ship passengers consuming raw oysters while visiting an oyster farm in Prince William Sound, Alaska (McLaughlin et al., 2005). The outbreak investigation documented an increase of 0.21oC per year in the July-August water temperature since 1997, and reported that 2004 was the first year that the oyster farm water temperature exceeded 15oC in July. This event provides direct evidence of an association between rising seawater temperature and the onset of illness.

Warmer temperatures may allow infected host animal species to survive winters in larger numbers, increase in population, and expand their range of habitation, thus increasing the opportunity to pass infections to humans. For example, milder weather and less snow cover may have contributed to a large outbreak of Puumala virus infection in northern Sweden in 2007. Puumala virus is endemic in bank voles, and in humans causes hemorrhagic fever with renal syndrome (Pettersson et al., 2008). Similar outbreaks have been noted in the Russian Federation (Revich, 2008). The climate-related northern expansion of the boreal forest in Alaska and northern Canada has favored the steady northward advance of the beaver, extending the range of Giardia lamblia, a parasitic infection of beaver that can infect other mammals, including humans who use untreated surface water (Arctic Council, 2005). Similarly, warmer temperatures in the Arctic and sub-Arctic regions could support the expansion of the geographical range and populations of foxes and voles, common carriers of Echinococ-cus multilocularis, the cause of alveolar echinococcus in humans (Holts et al., 2005). The prevalence of alveolar echinococcus has risen in Switzerland as fox populations have increased in size and expanded their geographic ranges into urban areas (Schweiger et al., 2007). Alveolar echinococcus was common in two

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regions of northwestern Alaska prior to 1997. Disease in humans was associated with contact with dogs; however, improvements in housing and dog lot management have largely eliminated dog-to-human transmission in Alaska. This may not be the case, however, in other parts of the Arctic where human infections with Echinococcus granulosis, and E. multilocularis are still reported, particularly in association with communities dependent on reindeer herding and dog use (Castrodale et al., 2002; Rausch, 2003).

Climate change may also influence the density and distribution of animal hosts and mosquito vectors, which could result in an increase in human illness or a shift in the geographical range of disease caused by these agents. The impact of these changes on human disease incidence has not been fully evaluated, but there is clearly potential for climate change to shift the geographical distribution of certain vector-borne and other zoonotic diseases. For example, West Nile virus entered the United States in 1999 and in subsequent years infected human, horse, mosquito, and bird populations across the United States and as far north as northern Manitoba, Canada (Parkinson and Butler, 2005). In the Russian Federation infected birds and humans have been detected as far north as the region of Novosibirsk (Revich, 2008). Although there is, at present, insufficient information about the relationship between climate and the spread of West Nile virus, a number of factors may contribute to its further northward migration. Milder winters could favor winter survival of infected Culex spp. mosquitoes, the predominant vector of West Nile virus, which since the 1970s have migrated as far north as Prince Albert, Saskatchewan in Canada. Longer, hotter summers increase the transmission season leading to higher numbers of infected mosquitoes and greater opportunities for human exposure. Climate change may alter the disease ecology and migration patterns of other reservoirs such as birds. These factors may affect disease incidence and result in expansion of the range of other arthropod vector-borne diseases.

A number of mosquito-borne viruses that cause illness in humans circulate in the U.S. Arctic and northern regions of the Russian Federation (Walters et al., 1999). Jamestown Canyon and Snowshoe Hare viruses are considered emerging threats to the public health in the United States, Canada, and the Russian Federation, causing flu-like symptoms and central nervous system diseases, such as aseptic meningitis and encephalitis (Walters et al., 1999). Sindbis virus also circulates in northern Europe. The virus is carried northward and amplified by migratory birds. In the late summer, ornithophilic mosquitoes pass the virus onto humans causing epidemics of Pogosta disease in northern Finland, an illness characterized by a rash and arthritis (Kurkela et al., 2008). In Sweden, the incidence of tick-borne encephalitis (TBE) has substantially increased since the mid-1980s (Lindgren and Gustafson, 2001). This increase corresponds to a trend of milder winters and an earlier onset of spring, resulting in an increase in the tick population (Ixodes ricinus) that carries the virus responsible for TBE and other potential pathogens (Skarphédinsson et al., 2005). Similarly in north-

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eastern Canada, climate change is projected to result in a northward shift in the range of Ixodes scapularis, a tick that carries Borrelia burgdorferi, the etiologic agent of Lyme disease. The current northern limit of Ix. scapularis is southern Ontario including the shoreline of Lake Erie and southern coast of Nova Scotia. Some temperature-based models show the potential for a northward expansion of Ix. scapularis above 60oN latitude and into the Northwest Territories by 2080 (Ogden et al., 2005). However, it should be noted that tick distribution is influenced by additional factors such as habitat suitability and dispersal patterns which can affect the accuracy of these predictions. Whether or not disease in humans is a result of these climate change-induced alterations in vector range depends on many other factors, such as land-use practices, human behavior (suburban development in wooded areas, outdoor recreational activities, use of insect repellents, etc.), human population density, and adequacy of the public health infrastructure.

Response to Climate Change in the Arctic

In 1992, the IOM published a report titled Emerging Infections: Microbial Threats to Health in the United States. This report uncovered major challenges for public health in the medical community primarily related to detecting and managing infectious disease outbreaks and monitoring the prevalence of endemic infectious diseases. It stimulated a national movement to reinvigorate the U.S. public health system to address the HIV/AIDS epidemic, the emergence of new diseases, the resurgence of old diseases, and the persistent evolution of antimicrobial resistance. In a subsequent report, the IOM provided an assessment of the capacity of the public health system to respond to emerging threats and made recommendations for addressing infectious disease threats to human health (IOM, 2003).

Because climate change is expected to exacerbate many of the factors contributing to infectious disease emergence and reemergence, the recommendations of the 2003 IOM report can be applied to the prevention and control of emerging infectious disease threats resulting from climate change. A framework for public health response to climate change in the United States has recently been proposed (Frumkin et al., 2008; Hess et al., in press). The framework emphasizes the need to capitalize on and enhance existing essential public health services and to improve coordination efforts between government agencies (federal, state, and local), academia, the private sector, and nongovernmental organizations.

Applying this framework to Arctic regions requires enhancing the public health capacity to monitor diseases with potentially large public health impacts, including respiratory diseases in children, skin infections, and diarrheal diseases, particularly in communities with failing sanitation systems. Monitoring certain vector-borne diseases, such as West Nile virus, Lyme disease, and TBE, should be priorities in areas at the margins of focal regions known to support both animal and insect vectors, and where climate change may promote the geographic

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expansion of vectors. Because Arctic populations are relatively small and widely dispersed over a large area, region-specific detection of significant trends in emerging climate-related infectious diseases may be delayed. This difficulty may be overcome by linking regional monitoring systems together for the purposes of sharing standardized information on climate-sensitive infectious diseases of mutual concern. Efforts should be made to harmonize notifiable disease registries, laboratory methods, and clinical surveillance definitions across administrative jurisdictions to allow comparable disease reporting and analysis. An example of such a network is the International Circumpolar Surveillance system for emerging infectious diseases. This network links hospital and public health laboratories together for the purposes of monitoring invasive bacterial diseases and tuberculosis in Arctic populations (Parkinson et al., 2008).

Public health capacity should be enhanced to respond to infectious disease food-borne outbreaks (e.g., botulism, gastroenteritis caused by Giardia lamblia or Vibro parahaemolyticus). Public health research is needed to determine the baseline prevalence of potential climate-sensitive infectious diseases (e.g., West Nile virus, Borrelia burgdorferi, Brucella spp., Echinococcus spp., Toxoplasma spp.) in both human and animal hosts in regions where emergence may be expected. Such studies can be used to accumulate additional evidence of the effect of climate change or weather on infectious disease emergence, to guide early detection and public health intervention strategies, and to provide science-based support for public health actions on climate change. The circumpolar coordination of research efforts will be important not only to harmonize research protocols, laboratory methods, data collection instruments, and data analysis, but also to maximize the impact of scarce resources and to minimize the impact of research on affected communities. Coordination can be facilitated through existing international cooperatives, such as the Arctic Council,14 the International Union for Circumpolar Health,15 and the newly formed International Network of Circumpolar Health Researchers.16

The challenge in the Arctic, however, will be to ensure sufficient public health capacity to allow the detection of disease outbreaks and monitor infectious disease trends most likely to be influenced by climate. The remoteness of many communities from clinical or public health facilities, and the harsh weather conditions of Arctic regions, often preclude appropriate specimen and epidemiologic data collection during an outbreak investigation, research, or ongoing surveillance activities. Staffing shortages are frequent in many in local clinics and regional hospitals that are already overwhelmed by routine and urgent care priorities, leaving little capacity for existing staff to assist public health personnel in outbreak investigations, research, or maintenance of routine surveillance activities.

14See http://www.arctic-council.org. 15See http://www.iuch.org. 16See http://www.inchr.org.

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Additional resources and training may be needed to ensure adequate staffing at these facilities, to address existing gaps between regional clinics and hospitals and public health departments, and to ensure a sufficiently trained staff to address the emerging public health impacts posed by climate change.

A key aspect of the public health response to climate change in Arctic regions will be the formation of community-based partnerships with tribal governments to identify potential threats to the community and develop strategies to address those threats. Communities at greatest risk should be targeted for education, outreach, and assessment of existing or potential health risks, vulnerabilities, and engagement in the design of community-based monitoring and the formulation of intervention strategies. The identification, selection, and monitoring of basic indicators for climate change and community health will be important for any response to climate change at the community level (Furgal, 2005). The selection of site- or village-specific indicators should be guided by local concerns and may include activities such as the surveillance of a key wildlife or insect species in a region where climate changes may contribute to the emergence of new zoonotic diseases or the measurement of weather (i.e., precipitation and temperature), water quality (i.e., turbidity, pathogens), and gastrointestinal illness (i.e., clinic visits) in a community. Linking communities across regions and internationally should facilitate the sharing of standard protocols, data collection instruments, and data for analysis. These linkages will be important for the detection of trends over larger geographic regions, should enhance a community's ability to detect changes that impact health, and will allow the development of strategies to minimize the negative health impacts of climate change on Arctic residents in the future.

Conclusion

Resident indigenous populations of the Arctic are uniquely vulnerable to climate change because of their close relationship with, and dependence on, the land, sea, and natural resources for their cultural, social, economic, and physical well-being. The increasing mean ambient temperature may lead to an increase in food-borne diseases, such as botulism and gastrointestinal illnesses. An increase in mean temperature may also influence the incidence of zoonotic and arboviral infectious diseases by changing the population density and range of animal hosts and insect vectors. The public health response to these emerging microbial threats should include enhancing the public health capacity to monitor climate-sensitive infectious diseases with potentially large public health impacts; the prompt investigation of infectious disease outbreaks that may be related to climate change; and research on the relationship between climate and infectious disease emergence to guide early detection and public health interventions. The development of community-based monitoring networks with links to regional and national public health agencies as well as circumpolar health organizations will facilitate method

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standardization, data-sharing, and the detection of infectious disease trends over a larger geographic area. This capacity is essential for the development of strategies to minimize the negative effects of climate change on the health of Arctic residents in the future.

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