PHJ_20_Complete_Issue

Public Health Bayer Environmental Science Journal No. 20 February 2009

CLIMATE CHANGE We can’t stop climate change but we can find ways to reduce its scale and impact. Learning more about these effects is a key to being prepared. In many cases, climate change favors the spreading of vector-borne diseases and the children of the world will, as usual, bear the greatest burden.

PUBLIC HEALTH JOURNAL 20/20092 |

C O N T E N T

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Editorial

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Climate change and vector-borne diseases (VBDs)

Redrawing the epidemiology mapby David H. Molyneux

C O V E R S T O R Y

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C L I M A T E C H A N G E A N D V B D s / E U R O P E

Global warming will lead to extreme weather events like tropical storms.

4

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Tick-borne diseases in Europe

Influenced not only by climate changeby Sarah E. Randolph

Climate change, globalization and Leishmania infections

When sandflies move northby Horst Aspöck and Julia Walochnik

Background

Using the past to predict the futureby Bernhard Stribrny and Ulrich Kuch

Bayer Environmental Science

PUBLIC HEALTH JOURNAL 20/2009

C O N T E N T

C L I M A T E C H A N G E A N D V B D s / A M E R I C A S

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59Cover photos: Brand X Pictures (globe); WestEnd61

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CD-ROM

Climate change and mosquito- and tick-borne diseases in the United States

Potential impact on vectorsby Lars Eisen and Rebecca J. Eisen

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Climate change and future threats to public health – with special focus on Mexico

Time to take actionby Jorge F. Méndez-Galván

Implications for future human plague risk in the western United States

Climate impact on fleas and rodentsby Anna M. Schotthoefer and Kenneth L. Gage

Book review

Malaria: Educational tools

Notes

History: Lyme disease

Physicians of past centuries wore protective masks to avoid catching the plague from the air. They were unaware of the disease being mainly transmitted by the bite of fleas living on rodents.

58


K E Y F A C T S


Global surface warming and potential increase of vector-borne diseases

Anticipated global warming can be expected to have direct effects on the distribution of insects and ticks that transmit infectious diseases. They will increasingly find ideal living conditions in previously temperate zones: for example in Europe (particularly in Mediterranean regions) and in North America. Even tropical and subtropical latitudes are faced with growing risks as further warming induces disease-transmitting insects to move into higher altitude areas (e.g. in Kenya). The map shows a

scenario with projected surface temperature changes for the late 21st century1. The more intense the red color, the greater the projected temperature increase (see bar below). Also marked on the map are examples of vector-borne diseases (and their vectors) that already occur in these areas and might appear more often or migrate to new regions as temperatures rise2. In addition, diseases are mentioned that today still count as infrequent exceptions (such as malaria in southern Europe) – but could increase dramatically within a few decades.3

1 Projected temperatures (2090-2099) are relative to the period 1980-1999. Source: IPCC.

2 Diseases listed in alphabetical order.

3 Due to the multiplicity of interactions associated with the phenomenon of climate change (temperature, surface water, humidity, wind, soil moisture, deforestation) one cannot make any concrete predictions. In addition, one has to take into account the influence of increasing global travel and trade.The chart simply represents trends based on past and present scenarios.

0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 (°C)

CLIMATE INFLUENCED DISEASES

NORTH AMERICA Dengue (mosquitoes)Lyme disease (ticks)Malaria (mosquitoes)

West Nile fever (mosquitoes)(amongst others)


CENTRAL / SOUTH AMERICA

Chagas (Triatomine bugs)Dengue (mosquitoes)

Leishmaniasis (sand flies)Malaria (mosquitoes)

(amongst others)


EUROPEChikungunya (mosquitoes)

Dengue (mosquitoes)Leishmaniasis (sand flies)

Lyme disease (ticks)Malaria (mosquitoes)

Yellow fever (mosquitoes)(amongst others)

CLIMATE INFLUENCED DISEASESCLIMATE INFLUENCED DISEASES

AFRICA Dengue (mosquitoes)Malaria (mosquitoes)

Rift valley fever (mosquitoes)Sleeping sickness (tsetse flies)


ASIA / PACIFICChikungunya (mosquitoes)


Malaria (mosquitoes)(amongst others)

Adapted from IPCC, Climate Change 2007: Synthesis Report; Summary for Policymakers, Figure SPM.6, page 9. Boxes added by Public Health Journal.

Available as poster on the enclosed Public Health CD-ROM

Global surface warming and potential increase of vector-borne diseases

Anticipated global warming can be expected to have direct effects on the distribution of insects and ticks that transmit infectious diseases. They will increasingly find ideal living conditions in previously temperate zones: for example in Europe (particularly in Mediterranean regions) and in North America. Even tropical and subtropical latitudes are faced with growing risks as further warming induces disease-transmitting insects to move into higher altitude areas (e.g. in Kenya). The map shows a

scenario with projected surface temperature changes for the late 21st century1. The more intense the red color, the greater the projected temperature increase (see bar below). Also marked on the map are examples of vector-borne diseases (and their vectors) that already occur in these areas and might appear more often or migrate to new regions as temperatures rise2. In addition, diseases are mentioned that today still count as infrequent exceptions (such as malaria in southern Europe) – but could increase dramatically within a few decades.3

1 Projected temperatures (2090-2099) are relative to the period 1980-1999. Source: IPCC.

2 Diseases listed in alphabetical order.

3 Due to the multiplicity of interactions associated with the phenomenon of climate change (temperature, surface water, humidity, wind, soil moisture, deforestation) one cannot make any concrete predictions. In addition, one has to take into account the influence of increasing global travel and trade.The chart simply represents trends based on past and present scenarios.

0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 (°C)


NORTH AMERICA Dengue (mosquitoes)Lyme disease (ticks)Malaria (mosquitoes)

West Nile fever (mosquitoes)(amongst others)


CENTRAL / SOUTH AMERICA

Chagas (Triatomine bugs)Dengue (mosquitoes)

Leishmaniasis (sand flies)Malaria (mosquitoes)

(amongst others)


EUROPEChikungunya (mosquitoes)


Lyme disease (ticks)Malaria (mosquitoes)


CLIMATE INFLUENCED DISEASESCLIMATE INFLUENCED DISEASES

AFRICA Dengue (mosquitoes)Malaria (mosquitoes)

Rift valley fever (mosquitoes)Sleeping sickness (tsetse flies)


ASIA / PACIFICChikungunya (mosquitoes)


Malaria (mosquitoes)(amongst others)

Adapted from IPCC, Climate Change 2007: Synthesis Report; Summary for Policymakers, Figure SPM.6, page 9. Boxes added by Public Health Journal.

Bayer Environmental Science4 | PUBLIC HEALTH JOURNAL 20/2009

For the climate of the world, twenty years is an unbelievably short time relative to the history of our planet – yet many things can change, as current developments show. For the Public Health Journal, twenty years is an extremely long time, which I think we can look back on with some pride. With this edition, you hold the twen-

tieth volume of the Public Health Journal in your hands: an anniversary edition, so to speak. On the back cover of this journal we have collected together all the cover pages of previous editions. In each of these journals we included reports and case studies from all over the world focusing on pest-related health issues and particularly on vector-borne diseases.

The current issue highlights climate change together with socio-economic factors including population migration and examines their potential effect on the spread of vector-borne diseases. Since this is a particularly complex and intensely discussed theme, it takes up almost the entire journal. We are very pleased to have persuaded expert authors from respected scientific centers to contribute their views and to help us find balanced perspectives.

Until now, Public Health Journals have dealt with vector-borne diseases and the health problems primarily facing the third world. However, with climate change the risk of vector-borne diseases is becoming very real in developed countries as well. Vectors may extend into new areas, for example into Europe, or to higher elevations, such as Mexico City as climate change impacts. Extreme weather events also create beneficial conditions for vectors and evidence points to these becoming more frequent in future as a direct consequence of climate change.

I hope that by bringing together the latest information we can help improve aware-ness and understanding of the relationship between vector-borne diseases and climate change. I sincerely hope that it helps us to be better prepared for the fight against these diseases.

I wish you an interesting and stimulating read.

Dear Readers,

PASCAL HOUSSET Head of


E D I T O R I A L

Pascal Housset

Bayer Environmental Science PUBLIC HEALTH JOURNAL 20/2009 | 5

he climate of the earth is changing. In fact, climate has been changing throughout the

history of our planet. Periods with particularly low or high temperatures are widely known as ice ages and interglacial periods, or icehouse and green-house periods. Climate interacts with life on earth, the biosphere, and the biosphere in turn influences climate both regionally and on a global scale, in important and highly complex ways that are so far only partly understood.

During the last 700 million years, there were five major glacial periods. In part, these glaciations were involved in five major mass extinctions during the last 542 million years, some of which were caused by climate change, shutdown of oceanic currents, volcanic activity or the impact of meteor-ites. Today’s biological diversity is the result of recovery processes after the last mass extinction at the Cretaceous-Tertiary boundary about 65 million years ago. For example, this is when non-avian dinosaurs disappeared and mammals started to spread over the planet. Geologically, glaciations are documented in sedi-mentary sequences by glacial depositions such as tillites or dropstones, and greenhouse periods by evaporites such as salt deposits or coal seams (Figures on the enclosed

CD-ROM). The latest ice ages started 1.8 million years ago with the beginning of the Quaternary period, which is characterized by several cyclic changes of glaciations and interglaciations. These cycles are documented, for example in northern Europe, by ventifacts, sandblasted stones with highly polished faces that were exposed in the vicinity of Quaternary sand dunes, thus giving testimony of the past presence of arctic areas with little or no vegetation.

Climate controlling factors

The Quaternary glaciations lasted about 100,000 years and the corresponding interglaciations 10,000 to 30,000 years. Such cyclic climate changes are linked with the solar energy flux that reaches the earth. These Milankovic cycles are named after the Serbian astrophysicist who first described this

phenomenon. They are caused by the fact that the earth surrounds the sun on a more and then less elliptic orbit with a cyclicity of 100,000 years. Besides this, the angle of the earth’s axis relative to its orbit changes up to 3° every 41,000 years. And a wobbling of the earth on its axis as it spins, called precession, completes a cycle every 23,000 years. All these phenomena change the

Using the past to predict the futureScientists at the Biodiversity and Climate Research Centre use a wide range of the most modern methods to analyze and document past and present interactions between organisms, biodiversity and climate. These are used to predict possible impacts of climate change. Here, Bernhard Stribrny and Ulrich Kuch discuss some of these patterns and predictions.

Climate change and vector-borne diseases

T

B A C K G R O U N D

The authors: BERNHARD STRIBRNY, ULRICH KUCHBiodiversity and Climate Research Centre,

Frankfurt am Main, Germany

B A C K G R O U N D

solar energy input to earth by modifying the dis-tance and angle of the incoming solar radiation. Finally, the energy discharge from the sun itself, correlated with the occurrence of sunspots, shows a cyclicity of 11 years. In Greenland ice cores, these variations are recorded for the last 100,000 to 400,000 years by biological and geochemical proximity indicators for palaeoclimatic conditions, for example, plant pollen and isotope ratios.

These intensity variations of the solar energy flux are presumably amplified by the earth‘s climate system. This interaction is one of the major climate controlling factors on earth. It is linked with a major transportation system of solar energy by means of warm oceanic water currents, the thermohaline circulation or oceanic conveyer belt. The Gulf Stream is a well known example of such a warm ocean current transporting energy from the Gulf of Mexico to the Arctic Ocean. The chemical compo-sition of the earth’s atmosphere and the ability of the earth’s surface to reflect solar radiation, the so-called Albedo effect, are additional global players in the earth’s climate system. Depending on these conditions, solar energy can be absorbed in variable amounts by the oceans and land masses, or becomes trapped in the atmosphere.

The earth is thus a physical system with a natural energy budget that is approximately in equilibrium, balancing incoming energy from the sun against energy lost to space. In the atmosphere, the trapping of solar energy is achieved by so-called greenhouse gases such as H2O, CO2, O3, N2O and CH4. Without this greenhouse effect the average surface temperature on earth would be -18°C, not +15°C as commonly measured. Thus, life on earth as we know it would not have been possible without greenhouse gases.

A planet heating up

The earth’s atmosphere is mainly composed of 78% nitrogen, 21% oxygen, 1% argon, 1% water vapor and by trace gases such as 0.04% of carbon dioxide. Most of this carbon dioxide was produced by volca-nic activities as part of the global carbon cycle (sketch of the global carbon cycle on the enclosed CD-ROM). Volcanoes are still an important source of carbon dioxide, releasing about 0.25 gigatons of this greenhouse gas into the atmosphere every year. However, the volcanic contribution represents merely 1% of the annual man-made emissions pro-duced by burning fossil fuels (e.g. oil, gas and coal) and biomass, which amounts to about 27 gigatons. A further 220 gigatons of carbon dioxide world-wide are emitted by the decomposition of organic matter in forests and grasslands each year. This natural production is however balanced by natural carbon sinks, for example, by the sedimentation of carbonate rocks, or the fixation of carbon in soils and finally by the photosynthesis of plants and algae. On the contrary, man-made carbon dioxide emissions are not balanced by such sinks.

Human activity has thus increased the atmospheric content of carbon dioxide from 0.028% in pre-industrial times to the present level of about 0.4%. According to the 4th Assessment Report of the Intergovernmental Panel on Climate Change (IPCC 2007), most of the observed increase in global average temperatures since the mid-20th century is therefore very likely due to the observed increase in anthropogenic greenhouse gas concentrations.

Climate change and human health

The predicted climate change is directly and indi-rectly associated with a multitude of serious threats to public health. For example, rising temperatures are linked with an increased frequency and varia-bility of extreme weather events such as heat waves (often with droughts and wildfires), hurricanes and cyclones, and exceptionally heavy or long-lasting

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rainfall and floods, which in turn may be associated with outbreaks of gastrointestinal infections, vector-borne diseases, or snakebites. In addition to such highly observable catastrophic events, there are more gradual changes such as rising sea levels lead-ing to a reduction of available land surface, or gradual changes in precipitation and groundwater balances threatening water supplies. Each of these events and processes increases the vulnerability of human populations and their homes and liveli-hoods, and starts a chain reaction of public health problems that often culminate in the challenge of caring for large numbers of displaced people under harsh environmental conditions.

Losers and winners

At the same time, climate change also affects animals, plants and microorganisms and their eco-systems and the innumerable ways in which they support human life and health. In fact, climate change is considered to be a leading cause of the currently observed, massive loss of biodiversity, second only to human land use changes. Here again, these developments can be abrupt such as in the case of extinctions of species with narrow climatic adaptations and small geographic distribu-tions (e.g. cold-adapted species living on moun-tains), which are especially vulnerable to sudden changes in their environment. Alternatively, chang-ing climatic conditions can also lead to a gradual decrease in fitness, reproductive success and thus population decline. Another possibility is the natu-ral selection of particular variants that may be better suited to their changing environment, but result in a loss of genetic diversity that ultimately increases extinction risk.

However, there will also be many examples of winners of global warming and its associated regional climate changes: some species may expand their distributions into regions that previously had unsuitable conditions, other species may greatly increase their population size as temperatures rise or rainfall and humidity regimes change. Yet others

may profit because they manage to utilize the ecological niches that are no longer occupied by differently adapted or less resilient species, or because their natural enemies have become rare or extinct.

Vector-borne diseases

Ironically, many of the most notorious medically relevant animal species seem to fall into the catego-ry of winners of global warming. Often enough, the expansion of their geographic ranges into new regions is preceded or accelerated by human intro-duction as a consequence of trade and travel global-ization, as in the case of the globally invasive Asian Tiger Mosquito (Aedes albopictus) and other dis-ease vectors. In addition to their obvious role as competent vectors on “stand-by” for major tropical infectious diseases, their recombination with new host species in their newly colonized habitat is also of concern because it bears potential for the trans-mission of new or presently rare diseases especially among wild mammals and birds, and from wildlife to domestic animals and humans. Dissecting the patterns and processes that have, on various time-scales, shaped the present distributions of medically relevant animals is thus an important research priority; integrating this information and life history data to model and predict their ranges, population dynamics and public health significance under regional scenarios of future climate change presents even more of a challenge. But it is a challenge that we must take on in order to adapt our health systems and economies to those changes and to mitigate their negative consequences. Achieving these goals will require major and globally sustained research efforts that address the full multi-factorial complexity of the problem of pathogens, vectors and reservoir hosts under climate change conditions – from single genes to entire ecosystems.

Article (with references) on the enclosed Public Health CD-ROM. Here you can also find additional figures (dropstones, coal seam, ventifacts) and a schematic sketch of the global carbon cycle. Ph

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Redrawing the epidemiology map

Climate change and vector-borne diseases


Redrawing the epidemiology map

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Climate changes and the complex interplay of different factors foreseen in the next decades will have a profound impact on vectors and the diseases they transmit. Prof. David H. Molyneux from the Liverpool School of Tropical Medicine out-lines current discussions and points to possible future problems.


C O V E R S T O R Y


by higher temperatures (figure on page 13). These are driven by increases in greenhouse gas (GHG) emissions, of which CO2 is the most prominent: CO2 emissions rose some 80% between 1970 and 2004 (figure on the right). This can be attributed to anthropogenic activities. Methane and nitrous oxide are the other com-pounds contributing to greenhouse gases. The atmospheric levels of CO2 and methane in 2005 substantially exceeded the natural range observed

over the last 650,000 years. This is due primarily to the use of fossil fuels, although changes in land use provide a significant, albeit smaller, contribu-tion. However, deforestation is perhaps the most significant cause (see box on page 12).

Sensitive ecosystems will suffer greatest impact

The IPCC report (see book review on page 52) concludes by using “likelihood” measures. For example, human influences have very likely contributed to sea level rises, are likely to have contributed to changes in wind patterns and increased temperatures of extremely hot nights. They have more likely than not increased the risk of heat waves, areas affected by drought and the frequency of heavy precipitation events. The projections and scenarios are the issues that many public health scientists are particularly interested in, and form the basis of much discussion. These scenarios are based on climate model forecasting of expected GHG emissions, and consequently surface temperature changes. Atmospheric CO2 in 2005 was 379 parts per million (ppm) and all models, assuming there is no mitigation, predict a mean rise in surface temperature of between 2 and 3.5°C by 2100.

These are clearly model estimates, but the geo-graphical pattern of projection shows most impact in northern polar regions, South Africa, the Sahara, Asia and North and South America. The conse-quences of these changes have a particular impact on the most temperature sensitive ecosystems.

limate change is now widely accepted as one of the most serious risks facing human-

kind. There is also a broad global consensus that climate change is driven by human activities, and that the associated increase in greenhouse gases is accelerating. The prediction of the most recent summary report from the Intergovernmental Panel on Climate Change (IPCC) provides depressing reading, particularly for many of the least developed countries already struggling to alleviate poverty.

Increases in average air and ocean temperatures The phenomena most relevant to public health and particularly vector-borne diseases are the pro-jections of increased global temperatures. This might affect the range of insects and ticks that transmit infectious diseases of the tropics as well as in sub-tropical and temperate zones. However, there are a multiplicity of interactions associated with the phenomenon of climate change that affect human health. These arise particularly as a result of the social, economic and political conse-quences of the physical, environmental and bio-logical changes. All these will immediately impact on populations and communities.

The IPCC states that the warming of the climate system is unequivocally based on observations of increases in global average air and ocean tempera-tures, more melting of snow and ice, and rising sea levels. Indeed, 1995-2006 were the warmest years since records began in 1850. Evidence from all continents shows that ecosystems are affected

CThe author:

DAVID H. MOLYNEUX

Liverpool School of Tropical Medicine,

Liverpool, UK

Liverpool School of Tropical Medicine (LSTM)Founded in 1898, LSTM is a registered charity affiliated with the University of Liverpool, UK. In addition to being an international center of excellence for research, it has extensive links with organizations worldwide and is devoted to controlling diseases of poverty and improving tropical health.


CO2 from fossil fuel use and other sourcesCO2 from deforestation, decay and peatCH4 (methane) from agriculture waste and energyN2O from agriculture and others

These include terrestrial systems such as tundra, boreal and mountain systems; the Mediterranean ecosystem and tropical forests as precipitation declines; coastal ecosystems such as mangrove swamps and salt marshes. In marine ecosystems, the coral reefs and the polar regions are the ocean ecosystems most sensitive to warming.

Too little water or too much

Water resources in the drier regions of mid-lati-tudes will be reduced due to less rainfall and increased evapo-transpiration. Agriculture will be affected in low latitudes due to decreased water availability and competition for this resource. Populations in low lying coastal areas are threat-ened by sea level rises and increased risk of extreme weather events (for example in Bangladesh, Myanmar and the pacific islands).

The regions likely to be particularly affected are:

• The Arctic, because of the high rate of expected warming; • Africa, because of its lower adaptive capacity and projected climate impacts; • small island populations where there is high exposure of the population along coastal systems; • the megadeltas of Asia and Africa due to high populations, risk of sea level rise, and storm surges

associated with extreme events and consequent flooding.

The poorest are most vulnerable

The projected impacts will vary depending on the actual temperature rise, assuming that any mitiga-tion is only partially effective. In terms of broader impacts on the health of populations, it is self evident that the poorest are likely to be the most vulnerable. These populations have the highest exposure to infectious diseases. The broad catego-ries of impact on water, ecosystems, food, coasts and health are interactive and cannot be isolated. This is because any impact within these categories will have consequences for health and many impacts will be associated with changing patterns of vector-borne infections.

Changes in vector-borne infections

Such changes in vector-borne infections will be difficult to anticipate and predict, even with the increasingly sophisticated models available. No matter how valid such predictions might be, the impact of the social and economic consequences of global warming will have serious indirect impacts on the health of populations. For example, population migration as a consequence of extreme climate events will result in internally displaced

C O V E R S T O R Y

HIGHER TEMPERATURES are driven by increases in greenhouse gas (GHG) emissions.

Global anthropogenic GHG* emissions

* greenhouse gases

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Í Reforestation is associated with a rapid capacity of vectors to adapt to new climax vegetation. Examples of such adaptation are seen in South America where in Jari, Brazil, the vector Lutzomyia flaviscutellata of Leishmania amazonensis adapts (as do rodent reservoir hosts) to Pinus and Gmelina planta-tions. It is also true in West Africa where Glossina palpalis adapts to cocoa and coffee plantations in humid savan-nahs.

Î Forest-related activities increase or change exposure to vectors. Many activities asso-ciated with deforestation, mining, hydroelectric projects, road building, logging, mineral exploitation and agriculture profoundly influence the biology of vectors or potential vector populations (e.g. biodiversity). They also result in exposure of both local indigenous populations and migrants. One example is the impact of mining on malaria outbreaks associated with An. darlingi abun-dance. A second is the capacity of Lutzomyia spp. to bite humans and transmit Leishmania braziliensis when pristine habitat is disturbed by road building.

Ï Loss of forest results in elimination of some vectors. These vectors are dependent on shade, humidity and lower temperatures. Examples of vector loss due to deliberate habitat destruction or population pressure are: Simulium woodi in East Africa; Chrysops vectors of Loa loa in West Africa; Glossina

palpalis from riverine habi-tat in West Africa, and Glossina morsitans spp. from Zimbabwe, Nigeria and Uganda.

Deforestation affects vector-borne diseasesSix key generalities are identified as relating to vector-borne infections while deforestation takes place

Ê Determinants of infection are: Behavioral patterns of humans (e.g. settlement patterns and activity patterns in forests), animal reser-voirs (ability to adapt to peridomestic settings), vectors (biting timing in relation to human behavior, zoophily vs anthropophily, flight range of vector); and capacity to adapt to human dwellings.

Ë Forest ecosystems are highly biodiverse, a level of diversity replicated in the organisms and vectors. This is best demonstrated in neo-tropical Leishmania spp. and sandfly diversity, as well as in Trypansoma cruzi with its molec-ular diversity, number of triatomine vectors and mammalian host species.

Ì Different vectors respond in a similar way as regional change occurs. In West Africa, three groups of insects appear to have changed their distribution as aridity has increased over the last 3 decades. This will continue if unmit-igated climate change drives the savannah further south into the forest zones of Africa. Precisely documented changes in Simulium damnosum sp. complex distribution have been demonstrated by the Onchocerciasis Control Programme: the savannah cytospecies S. sirba-num and S. damnosum have extended to more southern river systems with increasing drought and loss of savannah habitat. The An. gambiae Mopti form is more abundant compared to other cytotypes in arid areas. This is due to a linear correlation between the Mopti chromo-somal form and the normalized distribution vegetation index (NDVI), a measure of green-ness (a surrogate for rainfall). Tsetse populations have similarly responded to aridity by moving south into more humid savannahs.

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populations, reduced food security and require-ments for emergency interventions on an increas-ingly large scale. In addition, conflicts related to water resource availability can be expected. Such events will undermine ongoing “chronic” develop-ment efforts to deliver on the Millennium Development Goals where health targets feature prominently.

The consequences of such scenarios on the ability of already stressed health services to provide for the populations is likely to be extremely limited.Current per capita expenditure on health is often less than US$ 10 per year in least developed countries.

Insects adapt rapidly

Among the earliest health consequences of average global temperature increase will be changes in distribution of insect vectors of disease. The reason for this is that insect populations are highly adaptable. The number of species of insect vectors (and insects themselves) are greater than any of the macrotaxa (excluding microorganisms) and

indeed are more biodiverse and hence adaptable to ecological change. This is due in part to shorter generation times and rapid reproductive rates.

Mosquitoes are the most widespread vectors

The infectious diseases transmitted by insects are viral, bacterial, protozoan and helminth infections. Mosquitoes of several genera are the most wide-spread and important groups of insects that transmit human diseases. This includes not only diseases with a high mortality and morbidity but also a high epidemic potential in previously unexposed populations. These diseases are found extensively throughout the tropics and also into the sub-tropics. Other vectors are: • Sandflies, which transmit leishmaniasis; • ticks, which transmit viral and bacterial diseases;

Continental temperature change

Temperature changes simulated by climate models using either natural (blue) or both natural and anthropogenic forcings (red).

ALL CONTINENTS are affected by higher temperatures. There is a broad consensus that this climate change is influenced by human activities.

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• tsetse flies, which transmit trypanosomiasis of humans (sleeping sickness) and livestock (nagana);• triatomine bugs, which are the vectors for the American trypanosomiasis chagas disease.

There have been several studies of the potential impact of climate change on these different systems, for example, the shifts in northerly or altitudinal tick distribution in Sweden and Canada. However, climate change itself cannot be specifi-cally associated with the observed changes in tick distribution and viral encephalitis transmitted by ticks. Humans also impact on the landscape, influencing both habitat and wildlife hosts of ticks. In addition, changes in human behavior may influence tick-human contact (see article “Tick-borne diseases in Europe” on page 18).

Dengue, chikungunya and mosquitoes on the move

Several studies on dengue have reported climate change effects on the ecology of the mosquito vector Aedes aegypti. However, the suggested

associations are not consistent. Since dengue is an urban disease and breeding sites of Aedes are typically artificial containers filled with unpolluted water, the spread of dengue could be associated with urban expansion. Climate based maps of Aedes aegypti (temperature, rainfall, cloud cover) do however appear to match the disease distribu-tion patterns. Expansion of dengue and the problems of its control will be driven by the expansion of urban environments where there is high rainfall. Additional factors are limited attention to environmental contamination and the clean up of containers that provide breeding sites. This is combined with the absence of any vaccine to protect vulnerable populations, given that vector control can only be an emergency response to outbreaks.

The increased range of the Asian tiger mosquito Aedes albopictus has been an increasing cause for public health concern. Since this species was found in southern USA in 1985, the species has spread as far north as Maine and into eastern Canada. In Europe it has been recorded in 12 countries. It is a known vector of dengue. More recently, it has been incriminated as a vector of chikungunya virus, an alphavirus originally described in Tanzania and then Asia. In recent

GLOBAL WARMING AND EXTREME CLIMATE EVENTS will lead to popula-tion migration, reduced food security and conflicts over water resources.

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years, this virus has been associated with out-breaks in the Indian Ocean (Reunion, Maldives and Sri Lanka: see PHJ No. 18, p. 45) and South Asia. The outbreak on Reunion in 2005/2006 was associated with A. albopictus and also a new chikungunya virus variant specific for this mos-quito.

Chikungunya was first recorded in Europe with an outbreak in Ravenna, Italy, in 2007 (see PHJ No. 19, p. 56). It appears to be continuing to spread, reaching Australia and Singapore. These changes in the distribution of a mosquito, as well as the spread of a virus that seems to have adapted and co-evolved with the mosquito, have raised serious public health concerns. The cause of these changes is likely to be multifactorial. Climate change and global warming are perhaps prominent candidates, together with globalization. More extensive popu-lation movement, and increased global trade permit mosquito eggs to be moved over large distances, exposing susceptible people to a new infection.

Malaria influenced by climate

Malaria represents one of the most challenging global public health problems. Caused by a protozoan parasite (Plasmodium falciparum)

transmitted by Anopheles mosquitoes, it is largely now confined to the tropics. Sub-Saharan Africa bears the largest burden of the public health problems – an estimated one million childhood deaths are attributed to malaria per year. Yet only limited progress has been made in its control, despite well-defined strategies being in place.

Malaria epidemiology and distribution in Africa is highly climate influenced due to the existence of very efficient and adaptable vectors of the Anopheles gambiae complex. Malaria transmis-sion is also temperature sensitive, since mosquito survival and parasite development for subsequent transmission is a critical factor in driving the epidemiology of malaria. Temperature and rainfall are also limiting factors in mosquito ecology.

Systematic reviews suggest that the El Niño southern oscillation contributes to the risk of malaria epidemics in South Asia and South America. A sea surface temperature and multi-model ensemble of seasonal climate forecasts suggest they could be used for forecasting malaria control in southern Africa. However, the role of climate change on the geographical distribution of malaria remains uncertain. This is particularly true in relation to highland malaria (malaria outbreaks at previously unrecorded high altitude transmis-sion sites). Additional factors in resolving these issues relate to the absence of good baseline data on malaria transmission and clinical data, the increased drug resistance in East Africa, and absence of vector control.

Some studies have reported warming trends in Africa compatible with a change that would affect transmission potential. In Kenya, malaria admis-sions in the highlands have been associated with rainfall and high maximum temperatures in the previous 3-4 months. A similar observation was made in Ethiopia in a study from 50 sites in the late 1980s and early 1990s.

IN MANY FLOOD AREAS, as here in Bangladesh, the population is particularly vulnerable to life-threatening vector-borne diseases.

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C O V E R S T O R Y


Generalist vectors adapting to changeGeneralist vectors play a dominant role in transmission. This concept can be applied to the vectors associated with ecological and environ-mental disturbances that will arise from climate-generated change. These “generalists” are closely associated with the expansion of vector-borne diseases and land use change, and include the various Anopheles sp. complexes, Glossina palpalis group of tsetse flies, Lutzomyia longipalpis sandflies as well as ixodid ticks. Generalist vectors are often closely associat-ed with reservoir hosts that act as food sources. They are inevitably “catholic” in their choice of hosts and live in close proximity to humans. The generalist vec-tor concept describes the characteristics of the tick Ixodes scapularis, a vector of Borrelia burgdorferi, the cause of Lyme disease in east-ern USA.

Increasing abundance of more efficient vectors A commonly observed phenomenon in areas of ecosystem change is differing ratios of Plasmodium vivax and P. falciparum. Several examples exist over a wide geographical range and timescale (Asia, Central Asia and Americas) where an increase in the proportion of P. falci-parum compared to P. vivax has occurred. This is associated with health system disruption, irrigation, forest loss, mining and migration. An increase in the abundance of more efficient P. falciparum vectors such as An. darlingi occurs as biodiversity is reduced through environmental degradation.

Water-associated vector-borne diseases As climate changes, water impoundments, irrigation projects and small dams will need to be monitored for changes in vector-borne

disease patterns. The surface area and, more particularly, linear distance available for water contact are several orders of magnitude greater for irrigation schemes and microdams than large-scale impoundments. This enhances the interface and exacerbates edge effects associated with water-related infections. Such impoundments

also provide more extensive shal-lower areas for larval breeding. However, the relationships between the factors that generate abundant mosquito populations (water, tem-perature, shade and impoundment type/larval habitat) and disease are generated by an interplay between factors. These include immunity,

nutrition, access to care and increased wealth (ability to pay for drugs/bednets). Vector-borne diseases closely associated with water bodies can also be categorized into two groups: Those that can produce rapid epidemic or acute resur-gences (malaria and Japanese encephalitis); and medium- to longer-term impacts (Guinea worm, schistosomiasis and filariasis).

Close contact with reservoir hosts amplifying infectionsIn the case of zoonotic infections the behavior of wild mammals or domestic reservoir hosts and the interactions between such hosts and humans represent the basis of epidemics. In addition, animal husbandry, including intensive livestock production, provides settings for amplification of infections (e.g. pigs and Japanese encephalitis). This provides an effi-cient interface for pathogen interchange with other reservoirs and humans. The interface of habitats provide the opportunity for local epi-demic expansion. Such areas include the forest edge, shorelines of water bodies, new human settlements in forest clearings, urbanization on desert fringes or irrigated agricultural settle-ments in deserts.

Closely associatedClimate change generated factors have an impact on vector-borne disease predictions

C O V E R S T O R Y


To date, there is no evidence that climate change has had an impact on malaria epidemiology in South America, or in the Russian Federation where P. vivax is the common malaria parasite. It is important to take into account the difficulties of malaria diagnosis, the poor reporting systems, the use of private providers in care provision, the amount of drug resistance and the history of vector control. These factors are significant in any attempt to define the relationship between malaria and climate change. There is, however, a certainty that malaria and Anopheles will be among the most sensitive measures of temperature driven change of all infectious diseases. The epidemiological changes that will be observed will be due to the adaptability of Anopheles.

Warmer winters help bluetongue virus spread north

In the field of vector-borne livestock diseases, the expansion of the range of bluetongue virus some 800 km further north in Europe provides a well-documented example of rapid distribution change over a decade (see page 57). The virus is found particularly in sheep, but also in other ruminants. It has become a cause for concern in northern Europe as the disease spreads. Global warming has been suggested as a reason for this expansion, since warmer winters have increasingly allowed the virus to persist over winter. This has been accompanied by the extension of the range of the main vector Culicoides imicola. As the virus has spread north, other indigenous Culicoides species have become vectors, thus expanding the range of its transmission. Culicoides, because of their small size can move long distances with the wind. Hence, if transmission can become established in new areas where there are susceptible Culicoides, the disease becomes difficult and expensive to control. Vaccination is the only viable strategy given the difficulty of controlling such an abun-dant vector.

Changes in vector-borne disease epidemiology will continue to occur as a result of population growth and anthropogenic driven climate change. The rate of change, frequency of occurrence and our capacity to predict the likely outcome will have a major impact on public health, particularly in those regions where the projected changes are the greatest.

To reach the Millennium Development Goals the current state of health systems in poor countries requires a far greater increase in resources than are currently available. Considering the predicted rate of extreme climate events driven by global warming, the capacity of the international community to respond and the capability of countries most affected to manage the consequences of these events are limited.

These conclusions suggest that while a greater understanding of the various scenarios will have undoubted value, the management of such chronic and acute crises will be extremely challenging.

CONCLUSION

Article (with references) on the enclosed Public Health CD-ROM. Here you can also find a summary report from the Intergovernmental Panel on Climate Change (IPCC).

THE BLUETONGUE VIRUS is found particularly in cows and sheep and is an

example for vector-borne lifestock diseases. For sheep the disease is often lethal.

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Bayer Environmental Science18 | PUBLIC HEALTH JOURNAL 20/2009 Bayer Environmental Science PUBLIC HEALTH JOURNAL 20/2009 | 19Bayer Environmental Science18 | PUBLIC HEALTH JOURNAL 20/2009 Bayer Environmental Science PUBLIC HEALTH JOURNAL 20/2009 | 19

Climate change cannot fully explain the variable, often dramatic, upsurge in

tick-borne encephalitis in Central and Eastern Europe. The emergence of this

and other tick-borne diseases also appears to be a surprising consequence

of the political transition with the end of Soviet rule. The multi-factorial causes

include abiotic and biotic environmental changes, and human behavior

determined by socio-economic conditions.

INFLUENCED NOT ONLY BY CLIMATE

CHANGE

Tick-borne diseases in Europe

Warmer weather and changes in life styles have led to more outdoor activities – which increases the risk of catching tick-borne diseases.

Photo left: Comstock

Bayer Environmental Science18 | PUBLIC HEALTH JOURNAL 20/2009 Bayer Environmental Science PUBLIC HEALTH JOURNAL 20/2009 | 19



ick-borne diseases (TBDs) are the most widespread and prevalent of

all medically significant vector-borne diseases in Europe. They have also shown the most dramatic increase in incidence over the past two decades. This is particularly well documented for tick-borne encephalitis (TBE), a potentially fatal viral infection trans-mitted by the abundant and ubiquitous tick Ixodes ricinus. The most striking upsurges occurred in most central and eastern European (CEE) countries in 1993. Although varying in degree, they coincided exactly with political inde-pendence after the collapse of Soviet rule. In Hungary and Croatia, however, there was a change in the reverse direc-tion, with a major decrease in incidence from 1997.

TBD systems are highly sensitive to climatic conditions: e.g. temperature determines the timing of the tick’s life cycle; and moisture stress inhibits host questing (searching) by ticks and there-by increases mortality rates. Since climate has supposedly changed over recent decades, it makes sense to test the intuitive idea that climate change has driven the emergence of TBE.

T

Increase in temperature in 1989

For all the faults inherent in meteoro-logical records from ground instru-ments, some patterns are so striking that they cannot be dismissed as artifacts of, for example, the urban heat-island effect. One of these is the increase in temperature that occurred in 1989. That year mean annual temperatures increased by approximately 1°C across most of Europe, with no trend either before (since 1970) or after this step change. Moreover, even more marked changes occurred in the spring. In the Baltic States, for example, temperatures at the end of April typically increased by up to 1°C in 1989 and a further 2-4°C in 1993. There is as yet no satisfactory explanation for this phenomenon,

The author: SARAH E. RANDOLPH

Department of Zoology, University of Oxford, UK.

TICK-BORNE INCIDENCE increased significantly, but to different extents, in 1993 in most central and eastern European countries. In Latvia, incidence then decreased again after 1998.

Tick-borne incidents in Latvia and Czech Republic

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although greater insolation through reduced particulate pollution in the atmosphere is one possible cause, espe-cially with the collapse of industry that accompanied the end of Soviet rule. Here we are more concerned with the possible effects than the cause.

Temperature change is particularly relevant to TBE, because the virus must be transmitted from an infected nymph to many infectible larvae feeding together on rodents. For this, larvae and nymphs must have synchronous sea-sons of host-questing activity, which is most likely where temperatures rise relatively rapidly in the spring. Then larvae, which require average daily maximum tem-peratures of ca. 10°C, may become active soon after nymphs, which need lower daily temperatures of around 7°C. This means a greater degree of co-feeding is possible. Theoretically, the observed increase in spring temperatures with-in existing TBE foci could have allowed thermal conditions to become consis-tently more permissive for synchronous activity by nymphal and larval ticks about ten days earlier in April. This, however, did not happen until 1993, and we would expect a time delay before a consequent upsurge in TBE incidence, longer than is seen in CEE countries. Also, it is not yet clear what effect, if any, this relatively minor change would have on the overall transmission poten-tial and therefore the abundance of TBE virus-infected ticks.

Likewise, the spread of ticks into higher altitudes and higher latitudes with warming conditions, certainly poses new risks of tick-borne diseases, but the relatively small size of human popula-

tions in these areas limits the impact of this on the continental scale.

Climate change – causal or coincidental?

Correlations between climate change and epidemiological events can always be found because climate change is the universal backdrop for all recent events of any type. Evidence for causality falters when we test whether the pat-terns of epidemiological change match those of climate change. One defining feature of TBE epidemiology is its heterogeneity in space and time evident in all CEE countries, but largely hidden when looking merely at national mean incidences. Analysis at finer spatial scales, for example for each of the 85 counties in Estonia, Latvia and Lithuania, reveals that the start point of the upsurge varied from 1990 to 1998. Furthermore, the increase in each

NOT ONLY THE DEVELOPMENT of the ticks, but transmission of the viruses they carry are closely linked to seasonal temperature.

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C L I M A T E C H A N G E A N D V B D s


mostly centered around homesteads.This allowed perennial weeds, shrubs and eventually young trees to take over in large areas of abandoned arable land. This habitat change, together with con-siderably lower use of pesticides once intensive farming ceased, could have allowed increases in the rodent trans-mission hosts for TBE virus. The Czech Republic and Slovenia were least affected in these ways, but changes in the use of woodlands, which cover about 40-60% of Estonia, Latvia and Slovenia, may have been significant. This includes the effects of different access, exploitation and husbandry practices in state-owned and private forests on the local risk of contact with ticks.

Biotic elements of the environment are fundamentally important for microbes that circulate among wildlife hosts. While national cattle herds (and

county ranged from 2.5- to 74-fold in Estonia, 3- to 34-fold in Latvia and 8- to 706-fold in Lithuania.This is irrespec-tive of the prior incidence, while in 10 Baltic counties there was no consis-tent change. Yet the pattern of climate change across the Baltics was remark-ably uniform, to such an extent that it cannot fully explain the variable epide-miological events of the 1990s.

Other environmental changes

A variety of other human-induced envi-ronmental changes, many originating in the socio-economic effects of political transition, could have acted synergisti-cally to increase the abundance of infected ticks. Particularly relevant are the variable shifts in land cover and land use. To different degrees in each CEE country, the state and collective agricul-ture that dominated during Soviet times reverted to small-scale enterprises

BESIDES CLIMATE CHANGE, numerous factors affect the incidence of tick-borne diseases: e.g. changes in agriculture and weekend trips to the countryside, changes in industrial infrastruc-tures, more sunshine due to less pollution, increases in wild deer populations, collecting mushrooms in the forest, etc.

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therefore grazed pastures) declined abruptly, except in Slovenia, goats gen-erally increased. This potentially offers better feeding opportunities to ticks in marginal grazing lands and increasing the risk of TBE virus transmission to humans via infected raw milk. Large wildlife hosts such as deer, elk and wild boar are essential to support tick populations. These have fluctuated in classical predator-prey cycles, possibly exacerbated by hunters turning away from wolves that had no food or com-mercial value. Overall the trend has been upwards across much of Europe since the 1980s. Long-term records of tick populations are rare, but where they exist, they indicate increasing abundance correlated with host densi-ties (with the appropriate delay).

Socio-economic factors

There are two sides to this interaction between tick-borne pathogens and humans, the risk imposed by the natural wildlife transmission cycles and the exposure of humans to that risk. As human infection most commonly occurs

through an accidental bite by an infected tick, the probability of infection depends on the density of infected ticks, and also the degree of contact between humans and those ticks in their forest habitats.

It is now clear that increased exposure of humans to infected ticks may have resulted from some of the socio-eco-nomic effects of political transition. The agricultural reforms, industrial decline and shift to market economies all led to increased unemployment, eco-nomic inequality and consequent changes in living conditions. With about half the households in the Baltic countries left without a regular income by 1999, many people turned to other ways of making a living. Some of these, such as subsistence farming, are likely to have brought them into closer contact with ticks in forests and rough land near to their homes. In contrast, the closer geographical and cultural proximity of the Czech Republic to western Europe facilitated trade and a relatively rapid move to market conditions, so unem-ployment initially remained lower. At the same time, improved material

WITH THE FOCUS ON TBDs IN EUROPE, socio-economic changes play an equally important role as increasing tempera-tures.

Tick-borne encephalitis in central and eastern European countries

The relative increase in tick-borne encephalitis (TBE) incidence in central and eastern European countries from 1993 was strongly correlated with poverty, as indi-cated by the proportional house-hold expenditure on food. In Lithuania (LT), Latvia (LV), Estonia (EE), Slovenia (SI) and Czech Republic (CZ), TBE occurs throughout each country; in Poland (PL), Slovakia (SK) and Hungary (HU), TBE occurs in only part of each country.

Reproduced, with permission, from Sumilo et al (2008) Reviews in Medical Virology 18, 81-95 © John Wiley & Sons.

Ratio of mean TBE incidence 1993-1998 to 1985-1990

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Article on the enclosed Public Health CD-ROM

Tick-borne diseases (TBDs) are commonly zoonotic, maintained by complex wildlife transmission routes that may become more or less threatening to humans with any one of a number of environmental changes. In this case it appears that the political revolution at the end of the 1980s had an abrupt effect on the living conditions of all “partners” within this disease system: virus, ticks, wild-life and humans. TBE emergence has been much more gradual, but unrelenting, in western Europe, which is also subject to socio-economic change, but more by evolution than revolution. This awaits a full analysis. Interestingly, it appears that the looser the economic constraints the more people responded to unusually mild weather throughout the summer and autumn of 2006, presumably undertaking more recreational outdoor activities. This (without any higher tick abundance) is thought to have caused a dramatic peak in TBE incidence that year in Switzerland, Germany, Slovenia and the Czech Republic. Weather variability, however, should not be confused with climate change.

CONCLUSION

welfare in parts of each population was reflected in increased car ownership. This allowed more weekend visits to country dachas and other recreation sites. This clearly increases potential exposure to ticks in forests, particularly when combined with traditional mush-room collecting. Indeed, a sociological survey in Latvia clearly identified mushroom and berry collecting as one of the highest risk activities amongst forest visitors, second only to forestry work.

If these suggested causal factors are correct, the differential degree of upsurge in TBE incidence should be correlated with different degrees of poverty in each CEE country. This is exactly what is seen. Two highly significant predictors of the relative increase in TBE from 1993 in each country are perceived poverty and the proportion of total expenditure spent on food. Both these factors are likely to have directly affected people’s daily activities. Thus Slovenia and the Czech Republic suffered relatively little, while morbidity was the highest in Lithuania and Poland.

Decreased incidence as well as emergence

By identifying the causes of TBE emer-gence correctly, people are empowered to take effective ameliorative action rather than seeing themselves as victims of climate change. Vaccination rates increased since 1993 in response to perceived risk in the Baltic countries.However, incidence has decreased by far more than can be accounted for by vaccination or naturally acquired immu-nity. The greater the incidence in each county, the more TBE declined from 1999, suggesting that people were aware of the risks and modified their

behavior accordingly. In Hungary, how-ever, the decrease from 1997 is thought by local public health officers to be an artifact of new funding arrangements for TBE diagnosis resulting in a decrease in the number of laboratory tests.

THE MORE PEOPLE are aware of the risks posed by ticks, the more careful they are – this counteracts increases in TBDs.

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he current biodiversity in any part of the world is the result of permanent climate vari-

ability. This can be particularly and convincingly demonstrated in the temperate and northern parts of the Northern hemisphere. Here, the past million years are characterized by a succession of glacial periods interrupted by interglacials.

Climate change and biodiversity

Presently, we are living in an interglacial period that began about 10,000 to 12,000 years ago, leading to an increase of the average tempera-ture by ca. 7°C (see figure on page 25). During the coldest periods of the latest (certainly not the last!) glacial, about 21,000 years ago, large parts of Europe, Asia and

WHEN SANDFLIES MOVE NORTH

T

Climate change, globalization and Leishmania infections

America were covered by huge glaciers with heights reaching up to two kilometres. As an example: the region where the city of Innsbruck (Austria) is today, was buried under a glacier of more than 1700 m, most probably covering all the surrounding mountains.

The largest part of central and eastern Europe was within the permafrost region (with permanently frozen soil thawed only superficially in the warmer season) and of tundra-like character with only

grassland and no forests. The rich biodiversity of the previous interglacial period had

disappeared, it became extinct or survived in refugial areas, mainly in Mediterranean regions (see figure on page 27). After the end of the latest

glacial period, central and northern Europe (as

Leishmania infections show a great variety of clinical manifestations and cause about 60 000 deaths per year. They are increasingly gaining attention. This is particularly true with respect to a possible spread into northern regions due to global warming. Although certainly a justified consideration, presently globaliza-tion plays a significantly more important role. It is, however, assumed that further global warming in this century will lead to considerable spread of sandflies, the vectors of Leishmania, and thus probably also to human infections.




well as the northern parts of Asia and America) were gradually recolonized from the south, in Europe mainly from Mediterranean refugial centers and/or from the east. During this period, the Holocene, there was again a remarkable fluc-tuation in temperature, with two particularly warm periods (Holocene optimum) ca. 6500 and 4500 years ago. Most probably the glaciers in the Alps disappeared totally and the timberline was consid-erably higher than today.

During that period an extensive and intensive (re-) immigration of animals, plants, fungi and also microorganisms took place. Some of them reached the northern parts of central Europe and even Scandinavia, but some died out again a few hundred years later. However, some of them also found suitable conditions during later colder periods and survived until today. This is a very important fact, also with respect to vectors of pathogens and in particular sandflies, the vectors of leishmaniae.

Thus, climate change (or climate variability) is a very common natural phenomenon. This is why the global warming observed in the forth quarter of the past century was first regarded as a short momentary and transitional period within the post-glacial variation. However, after years of critical reluctance and intense discussions it has become clear now that climate change and in particular global warming exceeding the natural variation is a reality. The concentration of CO2 in the atmo-sphere has reached values that have not occurred throughout the past 650,000 years. Since we have no possibilities to reduce the global CO2 concen-trations within this century, even if a totally unrealistic stop of further greenhouse gas emission could be achieved, a further increase in the average global temperature is a fact.

There is no question that this will greatly influence the biodiversity composition of large parts of the earth. In particular, accelerated immigration of Mediterranean elements into central Europe is to be expected. Moreover, those thermophilic

Fluctuation of postglacial temperature

Weichsel/Würm glacial period “Little Ice Age”

“Atlanticum I, II”(Holocene climatic optimum)

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Increase of biodiversity: remigration and immigration

THE LATEST GLACIAL ENDED roughly 10,000 years ago. Presently we are living in an inter-glacial period. But the climate change in our time is exceeding the natural phenome-non of climate vari-ability.M

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organisms presently occurring in central Europe, but restricted to small, particularly favorable bio-tops, will spread and enlarge their distribution areas. This will also be of striking significance for the distribution of disease vectors. It is therefore irresponsible to deny the problem of climate change and not to consider adequate measures against emerging infectious diseases correlated with global warming.

Globalization and its impact on the spread of infectious diseases

Since Hominins started to migrate, they have con-tributed to the spread of pathogens. Homo erectus, in the course of the first out of Africa migration, brought their microorganisms to Asia, and this happened later permanent-ly – when Homo sapiens left Africa, when humans arrived in Europe and Australia, when they first invaded into America, and so on. In these cases, how-ever, the pathogens simply accompanied the migrat-ing human population into regions where no other humans lived. This changed significantly in historical times when humans migrated into parts of the world where other human populations were living. The introduction of infectious diseases by Europeans into America in post-Columbian times, with disastrous consequences for indige-nous populations, is a famous and sad example.

Already several thousand years ago people trans-ported goods from one country to another and also displaced vectors. Modern times have brought a tremendous acceleration and amplification of this phenomenon: millions of people travel over long distances every year – for business, education, or tourism, searching for better conditions, as refu-gees, etc. And billions of goods in containers or open, as well as farm, domestic and zoo animals

are transported from continent to continent by land, sea or air. Thus, there are numerous ways of displacing vectors and pathogens, particularly sandflies as well as leishmaniae by infected humans or animals, especially dogs.

Leishmania parasites cause leishmanioses

Leishmaniae (genus Leishmania) are eukaryotic unicellular organisms belonging to the eugleno-zoan taxon Kinetoplastida. Within the Kinetoplastida they constitute the sister taxon to the genus Trypanosoma, both belonging to the family Trypanosomatidae. Leishmania parasites were discovered almost simultaneously by William Boog Leishman and Charles Donovan. They were

both working on visceral leishmaniosis in India at the beginning of the 20th century. The first charac-terized species, described by Ross in 1903, was thus named Leishmania donovani.

The now more than 30 different species described can roughly be subdivided into four complexes: • The Leishmania don-ovani/infantum complex,

• the Leishmania major complex, • the Leishmania mexicana complex and • the Leishmania (Viannia) braziliensis complex.

However, there is no generally accepted system and new species continue to be described, as for example recently in Thailand. In Europe, the most prevalent “species” are genotypes 1 and 2 of the L. donovani/infantum complex. These two geno-types are also found in Latin America, where they were introduced during post-Columbian colonization. The other four gentoypes of the L. donovani/infantum complex occur in Africa and India. The L. major complex, including also

The authors: HORST ASPÖCK, JULIA WALOCHNIK

Department of Medical Parasitology,Clinical Institute of Hygiene and

Medical Microbiology, Medical University of Vienna (MUW), Austria



L. tropica and L. aethiopica, is widely distributed in the Old World, with L. tropica being the pre-dominant species in Central Asia, Asia Minor and in the Balkan peninsula. The L. mexicana complex and the L. (Viannia) braziliensis complex both occur exclusively in the Americas. However, while the L. mexicana complex is assumed to derive from an introduction of L. major to northern America via the Behring route in the Pliocene, the species belonging to the L. (V.) braziliensis com-plex are probably the only truly autochthonous American leishmaniae – that may have developed after the split of Gondwana in the Mesozoic. These are now usually classified as an independent subgenus or even genus (Viannia). It may be questioned whether the taxonomic status of spe-

cies is justified in many of these morphologically totally uniform strains.

Visceral leishmaniosis is usually lethal without treatment

Leishmaniae are transmitted by sandflies (Phlebotominae), Phlebotomus spp. in the Old World and Lutzomyia spp. in the New World. All representatives of the genus Leishmania exhibit two different life cycle stages (see figure on page 29). One is an elongated, flagellated so-called promastigote stage (length including flagellum: ~25 µm) living extracellularly in the gut of the phlebotomine vector. The other an oval “non-

DURING THE COLDEST PERIODS of the latest glacial (about 21,000 years ago) large parts of Europe were covered by huge glaciers: Scandinavia, almost the whole British Isles, northern parts of Germany, the Alps, the Pyrenees, and several other mountain ranges. The remaining permafrost region (central and eastern Europe) had a tundra-like charac-ter with poor biodiversity.

Europe about 20,000 years ago during the Weichsel/Würm glaciation

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flagellated” amastigote stage (3-5 µm) living intra-cellularly within macrophages and other cells, particularly of the immune system, in vertebrate hosts (many species of various families: rodents, dogs, ungulates and humans). Both stages have one single nucleus and one single mitochondrium, the latter harboring the kinetoplast, a DNA containing organelle characteristic for the Kinetoplastida.

cally manifest, the patients suffer from nausea, anorexia, diarrhea, weight loss and high fever. In the progressed state almost any organ can be affected, the most characteristic symptom being splenomegaly. Without therapy the disease is usually lethal within 1-3 years after onset of symptoms. An HIV infection enhances the risk of developing clinically manifest VL by 100 to 1000 fold. It is estimated that almost 10% of the AIDS patients in southern Europe will develop VL within the next few years, which makes leish-maniae the second most important opportunistic parasites after Toxoplasma gondii. Moreover, in immunosuppressed individuals the disease very often takes a more fulminant course and shows unusual symptoms.

CL can progress in very different forms, from a localized form to a diffusely progredient form, depending not only on the strain but also on the immune status of the patient. The most severe and occasionally also lethal form of CL is disseminat-ing mucocutaneous leishmaniosis caused by various representatives of the L. (V.) braziliensis complex. The countries with the highest inci-dences are Afghanistan, Iran, Saudi Arabia and Syria for the localized form, and Brazil and Peru for the progredient form. After an incubation period of several weeks up to even 3-4 months (L. tropica) the disease starts with a lesion around the site of infection. As sandflies are nocturnal insects the most affected body sites are the face and extremities. While the localized form usually – and even without therapy – heals within less than a year, the progredient form leads to a gradual destruction of the skin, cartilage and even bone if left untreated.

Diagnosis and treatment

The standard diagnostic technique for leishmani-oses is examination of stained smears and tissue sections. Alternatively, leishmanial antigen can be detected in clinical specimens, e.g. a commercially available test can detect Leishmania antigen in urine. In the recent past PCR (Polymerase Chain Reaction) and also real-time PCR have gained more and more importance for routine diagnostics.

Two different disease entities are caused by leish-maniae: visceral leishmaniosis (VL) and various forms of cutaneous leishmaniosis (CL). Worldwide around 12 million people are infected with Leishmania spp. and 350 million are assumed to be at risk of an infection. About 1.5 million new cases of CL and ca. 500 000 new cases of VL occur every year. 60 000 people die from leish-maniosis (predominantly from VL) annually. Autochthonous Leishmania infections are known from at least 88 countries.

VL is endemic in at least 60 countries around the world and is primarily caused by representatives of the L. donovani/infantum complex. The most affected countries are India, Nepal, Bangladesh, Sudan and Brazil (see figure on page 30). The incubation period is highly variable and an infec-tion can also persist without any symptoms. Typically children, but in particular also immuno-suppressed persons develop a more severe disease than healthy adults. If the infection becomes clini-

CUTANOUS LEISHMANIOSIS starts with a lesion around the infected site, usually on the face or limbs exposed to sandflies during the night. 60,000 people die from leishmaniosis every year.

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Targets for molecular diagnostics are usually the kinetoplast DNA (kDNA) or the ribosomal DNA (rDNA). PCR can be performed with bone marrow, blood and generally also with skin biopsies. However, in CL the achieved sensitivity is clearly below 100%. Serological tests are high-ly sensitive only for VL, for example those based on detection of IgG against the leish-manial antigen K39 can be applied for the rapid diagnosis of VL.

For therapy, the most common drugs are pen-tavalent antimony compounds. However, these can have severe side effects and meanwhile a resistance problem has also arisen in several regions. Alternative drugs are amphotericin B, itraconazole and allopurinol for systemic, and paromomycin for topical application. Miltefosine, an alkylphosphocholine, is a relatively new alter-nate drug that has the great advantage of oral and topical formulations.

Generally, it is assumed that even after successful therapy some leishmaniae do survive and persist within the host. This of course is not only relevant in the case of acquired immunodeficiency, but also for epidemiology, since these hosts can then func-tion as reservoirs for new infections. Particularly dogs play a significant role as reservoir hosts, also for several years now in central Europe.

Leishmanioses as emerging diseases

There is increasing evidence of the emergence of autochthonous, or naturally transmitted, leish-manioses in regions where the disease was only previously known in travellers returning from tropical or subtropical regions. This has created a strong demand to monitor the situation. If such cases emerge in northern regions where autochtho-nous leishmanioses had never been known before, one is primarily inclined to see a causal connection with global warming. This may be an error, although such a correlation may (most probably will) be of significance in near future. The cases of autochthonous leishmanioses in Germany are good examples.

Until 1999, it was believed that Phlebotominae represent faunal elements of low expansivity restricted almost entirely to Mediterranean coun-tries, and that they do not occur in Germany. Apart from several records in southern, south-western and south-eastern border regions, the occurrence of sandflies in central Europe was unknown.

In 1999, Phlebotomus mascittii was found in the southwest of Germany and in the following years further searches for sandflies in Germany were successful. Climate change and global warming was the first explanation for the surprising detection of sandflies in Germany. Further studies on the distribution of Phlebotomus spp. in extra-mediter-ranean countries revealed old records in eastern France located about 100 km away from the recent

LIFE CYCLE of Leishmania spp. In most species various vertebrates, e.g. dogs, rodents etc., maintain the circulation. However, humans are highly suscep-tible hosts and may contribute to the circulation.

1 Peritrophic membrane: a membrane containing chitin and proteins that surrounds lumen of midgut thus separating food from wall of midgut.2 Proboscis: elongated mouth parts adapted for sucking.

➊ Sandfly takes a blood meal (injects promastigote stage into the skin) (i)

➋ Promastigotes are phagocytized by macrophages

➌ Promastigotes trans-form into amastigotes inside macrophages (d)

➍ Amastigotes mul-tiply in cells (including macrophages) of various tissues (d)➎ Sandfly takes a

blood meal (ingests macrophages infected with amastigotes as well as free amastigotes)

➏ Amastigotes are liberated in gut

➐ In midgut amastigotes transform into promastigotes which multiply inside and outside peritrophic membrane1

➑ Promastigotes migrate to proboscis2

Vertebrate stagesSandfly stages

(i) = infective stage(d) = diagnostic stage



detection area. Thus, it was reasonable to assume that all these records of detection can be traced back to the same immigration. The Rhône-Rhine valley is a well-known route for Mediterranean organisms migrating northwards during periods of a warmer climate. Probably, sandflies already migrated into regions north of the Alps long ago (presumably during the Holocene optimum), colo-nized larger parts, but disappeared again when the climate cooled down – except for a few small areas where ecological conditions remained sufficiently favorable throughout the following millennia.

Today, at least four species of Phlebotominae have been recorded in central Europe and adjacent extra-mediterranean regions: Phlebotomus (Transphlebotomus) mascittii was found in vari-ous parts in Baden-Württemberg and recently also in Belgium. Prior to these findings the species was known from Switzerland and France. Phlebotomus (Larroussius) perniciosus was recently found in Rheinland-Pfalz in the west of Germany. The species was known from various parts of Switzerland and of northern Italy. Phlebotomus (Larroussius) neglectus was found in various parts

of Italy, in Hungary, and in Greece. So far, there are no records from central Europe north of the Alps. Ph. perniciosus is a confirmed vector of Leishmania spp., while Ph. mascittii is strongly suspected of transmitting Leishmania, although this has not yet been proven experimentally.

However, sandflies alone do not cause leish-manioses. So the question was where do the leish-maniae come from. Again it was not climate change, but an interesting facet of globalization. Leishmaniae are frequent parasites of dogs in Mediterranean countries. In some areas 25% to 50% of dogs, and as high as 90% of stray dogs are infected. Many of them develop clinical symptoms that are very conspicuous and lead to a miserable appearance. Many of these dogs were brought to central Europe, particularly to Germany, by compassionate tourists, ultimately leading to the development of a lucrative market. In fact, dogs suffering from leishmaniosis are offered for sale via the Internet, and there is a surprisingly high number of people, particularly in Germany, who buy such dogs and bring them – often illegally – home. According to conservative estimates about 20,000 dogs infected with Leishmania are pres-ently living in Germany, meaning the probability

Cutaneous leishmaniosis Visceral leishmaniosis Both varieties of leishmaniosis

ENDEMIC LEISHMANIA INFECTIONS are today mainly confined to tropical and subtropical regions, but are gradually spreading into temperate zones.

Geographical distribution of human Leishmania infections



Article (with references) on the enclosed Public Health CD-ROM. Here you can also find a selection of photographs showing clinical manifestations of the disease.

There is no doubt that the emergence and increase of Leishmania infections will become a particularly important consequence of global warming in the near future. Moreover, it is very likely that other pathogens transmitted by sandflies will emerge in parts of the world where they had never occurred before, in par-ticular, phleboviruses causing Pappataci fever and other acute febrile infections in humans. Since global warming has now been recog-nized as a reality, we have to monitor the situ-ation with respect to the emergence of infec-tious diseases very carefully. To do otherwise would be irresponsible.

CONCLUSION

that an infected dog is bitten by a sandfly is high enough to give rise to a Leishmania focus. But also horses, cats and other domestic animals are transported and imported into Europe, and these animals may also play a role as reservoir hosts. Moreover, a focus of Leishmania can be main-tained by a circulation of parasites between sand-flies and rodents. Thus, the emergence of Leishmania infections in central Europe is a result of globalization rather than climate change.

Temperature is the key factor

Naturally transmitted Leishmania infections are increasingly observed in humans as well as in domestic animals in various parts of the world, in particular in regions north of the classical distribu-tional areas of leishmanioses. This can be traced back to two key factors: Phlebotominae have been found in northern regions where they were appar-ently overlooked so far. It is very unlikely that the occurrence of sandflies in these areas is to be traced back to recent immigrations due to global warming. The second factor is the introduction of leishmaniae by infected domestic animals, in particular dogs, into those areas where sandflies capable of transmitting Leishmania spp. occur, as well as by infected humans coming from tropical or subtropical regions. Presently, the growing distribution areas of Leishmania are predomi-nantly a consequence of various forms of globalization. Since global warming is an evidence-based fact, and the increase of the average temperature by 3°C by the end of the century is a very reasonable assumption, it is to be expected that the distribution areas of several Phlebotominae species will grow considerably.

In a joint project we analyzed the climatological parameters of localities in central Europe and adjacent extra-mediterranean regions where sand-flies were found and compared them with the climatological data of Austria. Our analysis showed that temperature represents the key factor. However, in Austria the critical temperatures necessary for the species’ development are

presently not being fulfilled in either July or January. Nonetheless, an increase of temperature by only 1°C would lead to conditions allowing the occurrence of several Phlebotomus species in large parts of Austria. Those regions that would become particularly suitable for sandflies in Austria are the Rhine and Danube valleys, the eastern parts of the province of Burgenland and the border region with Slovenia. The species most likely to be expected are Ph. mascittii in western parts of Austria (winter temperatures are not high enough at present) and Ph. neglectus (summer temperatures are not yet high enough) in the east. A precondition would then be either the natural immigration or the (unintentional) introduction of sandflies into those parts of Austria, but once a population has become established, pathogens could be transmitted by the sandflies. This would mean the preconditions for increasing cases of Leishmania infections would be fulfilled in much larger regions than today.



POTENT IAL IMPACT ON VECTORS

Climate change and mosquito- and tick-borne diseases in the United States

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he increasingly recognized trend of ongoing climate change related to human activi-

ties has provoked much interest in how this will potentially impact vector-borne and other infectious diseases in the future. Studies are now focusing on climate-driven changes in spatial and temporal patterns of arthropod vectors and vector-borne diseases. Not surpris-ingly, this emerging research field has experienced some growth pains.

In the initial rush to generate risk projection scenarios for the coming decades, risk models were often developed based on the best available entomological or epidemiological data. In other words, not on data collected specifically for the purpose of deter-mining associations between climate factors and spatial patterns of vectors or vector-borne diseases. This produced a multitude of risk projection models based on empirical input data of vari-able quality. Certainly, the research field should continue to produce improved risk projections based on newly collected data. But it must

Increasing temperatures may result in mosquitoes or ticks invading or becoming more abundant at high altitudes or further north in the US. However, ongoing expansion of human populations into vector habitats or changes in human behavior also affect the risk of exposure to vector-borne pathogens. The authors conclude that climate change-driven effects on the numbers of vector-borne disease cases at the national scale in the US will likely be marginal in the 21st century.

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A WARMING CLIMATE could allow for invasion of ticks and mosquitoes into mountainous areas that now are too cold for them to gain a foothold. Ph

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expand in scope to also include a focus on generating hard evidence for climate change effects on vectors and vector-borne diseases. This needs to account for the relative roles of climate versus confounding factors, such as socio-economic conditions, to explain observed changes in vector-borne disease patterns.

There is a disturbing lack of empirical long-term studies that will allow us to demonstrate that future changes in risk of exposure to vectors and their associated pathogens were in fact driven by climate factors. Perhaps the best evidence that climate change can impact risk patterns for exposure to vectors and vector-borne pathogens comes from studies on the common tick, Ixodes ricinus, and tick-borne encephalitis virus (TBEV) in mountainous regions of the Czech Republic. A 25-year study conducted by Milan Daniel and colleagues along an altitude transect (from 650–1550 m above sea level) in the Krkonoše Mountains demonstrated the following changes from 1981-1983 to 2002-2006:

• Mean June-August monthly tempera-tures at 1000 m increased by 1-1.5°C; • the upper distribution limit for I. ricinus shifted from 700–800 m to at least 1100 m;• the upper limit for successful comple-tion of the tick’s life cycle shifted from below 700 m to 1100 m; and • TBEV was detected in 2005 from I. ricinus at 900-1100 m, where the tick was absent in the early 1980’s.

These findings not only provide strong evidence for climate warming-driven change in the spatial risk pattern for exposure to I. ricinus and TBEV. They also support epidemiological data suggesting that the altitude “ceiling” for TBE risk in the Czech Republic has increased in recent decades.

Need for studies combining vector and epidemiological data

When based on epidemiological data, retrospective studies of climate change effects on vector-borne diseases can be compromised by the location of resi-dence, rather than the location of the probable pathogen exposure site. Often the only spatial information available is from case files. For epidemiological data, location of residence, rather than location of probable pathogen expo-sure site, often is the only spatial infor-mation available from case files. This can compromise retrospective studies of climate change effects on vector-borne diseases. In the US, for example, pathogen exposure locations are rou-tinely determined for plague, which is a rare and severe flea-borne disease (see article on page 46). In contrast, the quality of information for potential exposure sites is highly variable for more common and less severe diseases such as tick-borne Lyme disease and mosquito-borne West Nile virus disease.

The authors: LARS EISEN

Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins,

Colorado, USA REBECCA J. EISEN

Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention,

Fort Collins, Colorado, USA



Use of epidemiological data for West Nile virus disease presents an addi-tional challenge, since many infections are asymptomatic or result only in mild fever, which is unlikely to be recognized and reported. Consequently, there is a critical need for prospective studies to more conclusively demonstrate that climate change can impact spatial epidemiological patterns. Such studies should focus on key areas where climate change is likely to impact spatial patterns of distribution or incidence of a given vector-borne disease. The studies should include determination of likely patho-gen exposure sites and account for potential confounding factors: e.g. expansion of human populations into risk habitats, or changes in human behavior leading to increased risk of vector and pathogen exposure.

Prospective epidemiological studies should also be complemented by collection of entomological data. This should include vector presence and abundance, and pathogen presence and prevalence in local vector populations. Entomological data are unequivocally linked to specific spatial locations (the collection sites). Therefore, it is possible to reliably track changes over time in risk of exposure to vectors and their associated pathogens along transects where climate change is likely to impact risk patterns.

We outline here potential effects of climate change in the coming decades for three vector-borne diseases in the US: tick-borne Lyme disease and mosquito-borne West Nile virus disease and dengue.

Lyme disease

Lyme disease is the most commonly reported vector-borne disease in the US, with more than 20,000 annual cases in recent years. Primary vectors of the Lyme disease spirochete Borrelia burgdorferi include: the black-legged tick, Ixodes scapularis, in the east; and the western black-legged tick, Ixodes pacificus, in the far west. The vast majority of cases are reported from two distinct geographical foci: the Northeast (Connecticut, Delaware, Maryland, Massachusetts, New Hampshire, New Jersey, New York, Pennsylvania and Rhode Island) and the Upper Midwest (Minnesota and Wisconsin) (see map above).

Dramatic effects on Lyme disease in the US are not expected under a scenario of climate change. The most likely effects are increases in tick vector abundance and risk of exposure to the Lyme dis-ease spirochete in the very far Northeast (Vermont, Maine and the upstate parts

Lyme disease in the United States

BLUEReported Lyme disease cases in the United States, 2006. One dot placed randomly within county of residence for each reported case.

ORANGEAreas in the Northeast with potential for increases in vector tick abundance under a scenario of climate warming. Note that orange areas were added to the CDC map by the authors and were not part of the original map.

Map from the Centers of Disease Control and Prevention website: http://www.cdc.gov/ncidod/dvbid/Lyme/ld_statistics.htm



of New Hampshire and New York). We may also see increased risk in the north-ernmost reaches of the Upper Midwest (far northern Minnesota and Michigan’s upper peninsula). Since these areas are sparsely populated, increases in local Lyme disease risk will not significantly impact national case loads. This is unless there is a corresponding shift in population demographics.

West Nile virus disease

West Nile virus was introduced to New York in 1999 and spread rapidly across the US. It reached the Pacific Coast, causing a disease outbreak in California in 2004. The virus has now established itself in enzootic bird-mosquito trans-mission cycles throughout the US. The number of annual reported West Nile virus disease cases appears to be stabi-lizing at around 3000-4500.

Vectors involved in enzootic transmis-sion or transmission of West Nile virus to humans include a wide range of Culex mosquitoes (e.g. Cx. nigripalpus, Cx. pipiens, Cx. quinquefasciatus, Cx. restuans, Cx. salinarius and Cx. tarsa-lis). Predicting the effect of climate change on risk of human exposure to mosquito vectors and West Nile virus in the US is a complicated undertaking.

Reeves and collaborators already noted in 1994 that climate warming would likely cause a northward shift in the distribution of Cx. tarsalis. This mos-quito is a key vector of West Nile virus and other arboviruses to humans in the western US. Climate warming could result in an expansion of the range of Cx. tarsalis into higher altitudes where the mosquito currently cannot establish stable populations. Increased summer temperatures could lead to shorter development times for the larval mos-quito stage. They also could result in a shorter extrinsic incubation period for West Nile virus in females (the time elapsing from the female becoming infected to being able to transmit the virus while feeding).

On the other hand, climate warming may result in reduced snow-pack and subsequent river and stream flooding activity. This could reduce available larval development sites for West Nile virus vectors. Further, human popula-tion sprawl and land use patterns will be critical confounding factors in studies of climate change effects on mosquito vectors and West Nile virus disease. This is especially true for naturally dry landscapes in the central and western US, where agricultural irrigation prac-tices and urban sprawl are creating

CULEX MOSQUITOES are key vectors of West Nile virus. The causative agent of Lyme disease, the most common vector-borne disease in the US, is trans-mitted by Ixodes TICKS.

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mosquito development sites and increased potential for human-mosquito contact.

Similar to Lyme disease we expect to see local climate change-driven effects on West Nile virus disease risk, but no dramatic changes in the number of reported cases at the national scale in the US. Most heavily populated areas already have well-established West Nile virus transmission cycles. Under a scenario of climate warming in the western US, Cx. pipiens and Cx. tarsalis may become established or more abundant at high altitudes in the Rocky Mountain region and in coastal areas of northern California, Oregon and Washington. On the other hand, these mosquitoes may lose ground in southern California, Arizona and New Mexico. Dengue

The potential for climate warming to result in range expansion and increased abundances of the yellow fever mosquito Aedes aegypti in the US has generated much interest. This scenario is, however, counteracted by housing quality and human behavior. In dengue endemic areas, transmission of dengue viruses is considered to predominantly occur indoors, where Ae. aegypti females preferentially rest and feed. The high quality of housing in the continental US, including window screens and air-condi-tioning, will likely act to prevent dengue virus transmission and thus mitigate the effect of potential increases in abun-dance of vector mosquitoes.

Mosquito and tick vectors in recreational areas of the Mountain west

The Colorado Front Range, which includes the transitional zone between

the Rocky Mountains and the Central Plains, provides a unique opportunity to study effects of climate change on several important vectors: The West Nile virus vectors Cx. pipiens and Cx. tarsalis and the Rocky Mountain wood tick, Dermacentor andersoni. The latter transmits the causative agents of Colorado tick fever, Rocky Mountain spotted fever and tularemia.

The Front Range is topographically and climatically highly diverse; Larimer County alone encompasses elevations ranging from 1450 to >4100 m. Habitats range from short-grass prairie in the east to montane and subalpine forests, and alpine areas to the west (see map above).

Cx. pipiens and Cx. tarsalis are abun-dant, and West Nile virus disease is hyperendemic, at low elevations (below 1800 m) in eastern Larimer County. These mosquito vectors are, however, virtually absent at high elevations in the western part of the county, including

Topography in Larimer County, Colorado

UNIQUE OPPORTUNITY to study effects of climate change on vector distribution

along elevation gradi-ents. West Nile virus vectors are currently

abundant at low elevations in Larimer County, while Rocky

Mountain wood ticks are found mainly between

2200 and 2350 m. Summer tempera-

ture increases could shift these vectors to higher elevation

patterns.

< 1750m

1750 - 2000 m

2001 - 2250 m

2251 - 2500 m

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2751 - 3000 m

3001 - 3250 m

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> 3750 m



Rocky Mountain National Park (see map on previous page: just west of Estes Park) which receives over 3 million visitors annually. This is an excellent example of a local area where climate warming may result in mosquito vectors expanding their ranges to higher eleva-tions and an arboviral disease becoming a public health problem in a heavily used recreation area.

Estimates based on associations between temperature factors and abundance of Cx. tarsalis in favorable habitats along elevation gradients in Larimer County, suggest that a summer temperature increase of 1-2°C could shift the upper limit of the mosquito distribution several hundred meters upward in elevation. Potential climate warming-driven changes for risk of exposure to Culex vectors and West Nile virus at lower elevations in heavily populated areas of eastern Larimer County are difficult to predict. On the one hand, increasing summer temperature could shorten

larval development times and extrinsic incubation periods for the virus, and would probably result in intensified West Nile virus transmission. But this could be offset by decreased availability of larval development sites due to shrinking snow-packs and spring flooding activity.

The Rocky Mountain wood tick pres-ents a different but equally intriguing scenario. The tick has a narrow climate range and can be found at mid-range elevations in Larimer County, with peak abundances around 2200-2350 m in montane forest habitats. Few host-seeking ticks are encountered below 2000 m or above 2500 m (see table on the right). Suitable tick habitat is pres-ent both below and above the elevation where tick abundance currently peaks. Based on associations between temper-ature factors and tick abundance in the Poudre Canyon elevation gradient in Larimer County, a 1°C increase in summer temperature could shift the

Dramatic effects of climate change on numbers of vector-borne disease cases will only occur in situations where abundances of infected vectors change drastically in heavily populated areas. Under a scenario of future climate warming, this is most likely to occur either at the southern or northern limits, or at the upper altitudinal limits of vector distributions. Perhaps the most frightening specific scenario in North America relates to climate warming-driven expansion of the yellow fever mos-quito, Aedes aegypti into higher elevations in Mexico. Located here are several large cities that currently are free of local dengue virus transmission, including Mexico City. Studies based on empirical field data for the mosquito vector are needed to determine if realistic climate warming scenarios could allow for establishment of Ae. aegypti in high elevation cities.

Could Aedes aegypti become established in Mexico City under a scenario of climate warming?

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Climate change-driven effects on the number of vector-borne disease cases in the United States will likely be marginal in the 21st century. Prospective long-term stud-ies should focus on local areas where climate change is likely to have significant effects on risk of exposure to vector-borne pathogens in coming decades. Examples of such areas are the far northeastern US for Lyme disease and the Rocky Mountain region for West Nile virus dis-ease. Future studies should include both entomological data (vector presence and abundance; pathogen presence and prevalence) and epidemiological data (including determining likely pathogen exposure sites). They also need to account for confounding factors such as expan-sion of human populations into risk habitats, or changes in human behavior leading to increased risk of vector and pathogen exposure.

CONCLUSION

Article (with references) on the enclosed Public Health CD-ROM.

area with peak tick abundance 100 m upwards in elevation. Colorado Front Range elevation gradients exemplify a situation where climate change is likely to have measur-able effects on spatial patterns of vectors and their associated pathogens in coming decades. Our challenge is now to recognize and exploit these types of “natural experiments” to empirically demonstrate that future observed changes in patterns of risk for exposure to vector-borne pathogens were in fact related to climate change. Ideally, this should be accompanied by similar stud-ies in areas where climate change is expected to have limited and minimal effects on risk of exposure to the same vector-borne pathogens. This should provide a balanced view of the overall effects of climate-driven change within the geographical ranges of the vectors.

RELATIONSHIPS between elevation and abundances of Culex tarsalis mos-quitoes (collected by CDC light traps baited by dry ice) and Dermacentor ander-soni ticks (collected by drag sampling of vegetation) in Larimer County, Colorado.

Elevation and abundance

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Elevation range with peak risk

Potential for increased risk under a warming scenario

Potential for increased risk under a warming scenario



Climate change, particularly extreme weather events, potentially increase

ecological conditions favoring the emergence, spread and establishment of

vector-borne diseases in the Americas. Although globalization and population

migration seem to play a major role today, preventative measures should be

applied for diseases that may become a threat in the future due to global

warming.

Time to take action

Climate change and future threats to public health

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ver the last few millennia, the climate has played a crucial role in regulating life on the

planet, creating spaces, frequencies and altera-tions in which living creatures have developed and specialized. Climate variations resulted in a great variety of life forms. Fluctuations in rainfall and drought, combined with earth movements led to the development of cold and warm climates, creating different regions throughout the planet. But these variations occurred regularly. They were not intense or sudden, although sporadic isolated climatic episodes of very intense rainfall or drought were observed such as El Niño. These phenomena are known as natural climate change. However, over the last 200 years and mainly in the last 50, the frequency and intensity of climate change have resulted from environmental modifications. Caused by society through the burning of fuels and changes in landscape mainly through agriculture, such environmental alterations result in a drastic modification of flora and fauna. These latest changes are known as anthropogenic or caused by humans.

For example, these new relationships may be produced by rainfall and changes in temperature patterns. Extreme phenomena are growing in intensity and frequency, with devastating hurri-canes, severe flooding and intense drought periods. These changes are also causing modifications in animal and plant life and, according to some predictions, the next 100 years could lead to as yet unguessable alterations. This is why it is very important to make every possible effort to under-stand what is happening and to look towards the future in order to mitigate or prevent, where possible, even more serious issues. In terms of health-related problems, vector-borne diseases (VBDs) cause some of the worst consequences. Malaria, dengue, Chagas disease, leishmaniasis, other arboviruses (Western Nile encephalitis, Eastern, Western and Venezuelan Equine

O Encephalitis, Japanese Encephalitis, Chikungunya, etc.) have already appeared in alarming numbers. Increases in these diseases are either related to climate change or else to other factors, so major changes may be expected in the near future.

Temperature, wind and rainfall forecast to rise

Climate changes have an impact on the environ-ment through four different sets of conditions:

firstly, on extreme weather events (frequency, severity and geography); secondly on ecosystems and in particular land and marine species; thirdly on the rise in sea level; and fourthly on environmental degradation. Some of the most important events occur in their extreme form, such as the increase in intense precipitation, across all latitudes, but particularly in the North and South American continent, northern Europe and northern and central Asia. Likewise, hurricanes or typhoons in the Pacific and Atlantic Oceans have intensified both in severity and number (see

figure on page 42). It is believed that forecasts of these changes and others such as rises in tempera-ture, wind and rainfall, are highly reliable.

It is quite obvious that changes in temperature, rainfall, vegetation and the changes seen through-out the planet lead us to expect major disease modifications. This not only applies to VBDs but also to disease spreading towards areas where they were non-existent in the past. They also point to accelerated rate of serotype mobilization or causal agent variety for various diseases, as well as the exchange of vectors among different continents.

However, it would seem that climate change has not yet substantially modified the behavior of diseases, particularly VBDs. Rather, the changes observed in diseases are more due to increased

The author: JORGE F. MÉNDEZ-

GALVÁN

Hospital Infantil de Mexico “Federico Gomez”, Mexico



exchange and to the frequency of such exchanges. This is due to economic dynamics in a world globalization context.

Globalization and migration spreading pathogens

The Medical Institute Workshop on the Impact of Globalization on the Emergence and Control of Infectious Diseases (National Academy of Sciences of the United States, 2006), concluded that the new threat in an economically globalized world includes the risk that infectious diseases may spread from their original prevalence areas to places where they did not exist in the past. This new context has evolved in a world of fast com-munication and easy access. This includes mass migration of rural populations to urban areas and between countries due to people seeking better employment and remuneration options. Between the 1970s and 1990s there was a substantial decrease in rural populations in developing coun-tries, with observed international legal and illegal migration towards developed countries. New trading patterns and international trade agreements

are contributing to the climate change scenario, increasing already prevalent risks. It is possible to foresee that this economic phenomenon has led to the fast adoption of more energy-hungry lifestyles that have a greater impact on climate change.

It is clear that major migration patterns are causing the mobilization of populations that are suscepti-ble to certain diseases, and are also spreading pathogens among various regions of the world. This is why the four dengue serotypes are spread-ing fast and steadily in decreasing cycles of eight to less than four years. The same applies to the emergence and spread of the human immunodefi-ciency syndrome throughout the world, or the rapid spread of resistant strains of the tuberculosis bacillus.

In a historical parallel, these movements of people seeking new economic options are not new; neither is the movement of bacteria. The major plagues that spread through Europe over millennia and the smallpox outbreaks in native communities of the Americas during the (European) conquest spring to mind. The latter infections played a major role in the colonizers’ success.

North Atlantic hurricanes and named storms (1884-2006)

HURRICANES AND STORMS severe enough to merit a name have risen and fallen in number over the last 60 years. But the gen-eral trend since 1995 has been continuously upward, reaching numbers well above those previously recorded.

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Named stormsHurricanes

1950 1960 1970 1980 1990 2000 2010




produce short-term outbreaks, mainly of malaria or dengue, although sometimes also Japanese encephalitis. Intense torrential rains and hurri-canes cause immediate flooding and result in an environment where temperature, relative humidity and mosquito breeding grounds increase the risk of diseases such as malaria, dengue, chikungunya, Japanese encephalitis, Rift Valley encephalitis, Western Nile virus or some rickettsias. It is timely to point out that another group of diseases such as zoonoses are becoming more important in post-disaster conditions, because wildlife as well as pets are also mobilized to safer areas. If these loca-tions coincide in time and place with leptospirosis or rickettsias hosts (rodents) or with hosts of other diseases, widespread or localized outbreaks can occur, and these are often highly lethal.

Malaria program in Mexico a success

However, climate change in itself cannot explain the epidemic behavior of VBDs so far. More precisely, a study of the incidence of diseases such as malaria in the Americas reveals that this has dropped in the last ten years (see Figure 2). In Mexico for example, there has been more than a

Extreme weather events cause disease outbreaks

Health and disease processes may be explained through the interaction of hosts (human and other animals), pathogens (viruses, bacteria and para-sites) and the environment (physical, biological, social). More specifically, factors determining the survival of disease vectors may be of two types:

• Abiotic factors such as temperature, rainfall, relative humidity, wind, solar radiation, topogra-phy and hydrology; and • vegetation changes caused by agriculture and forestry or by urban modifications – just to mention a few anthropogenic factors.

Most VBDs emerge with increased rain and tem-perature, particularly most of those spread by mosquitoes.

Although there have been reports of some changes in VBD trends as a result of climate change, it is probable that major modifications are still to come. However, it is important to mention that more frequent and intense extreme weather events such as torrential rains and hurricanes and typhoons

EFFECTIVE CONTROL PROGRAMS probably account for the general decrease in malaria cases in the Americas. For example, malaria is at the lowest level ever in Mexico.

RELATIVELY NEW TO THE AMERICAS, dengue hemorrhagic fever has been on the increase over the last ten years, often linked to the re-emergence of serotypes.

Fig. 2 Fig. 3

Malaria cases in the Americas (1994-2007) Dengue cases in the Americas (1980-2008*)

1,400,000

1,200,000

1,000,000

800,000

600,000

400,000

200,000

0

94 96 98 00 02 04 06 07

Year

30,000

25,000

20,000

15,000

10,000

5,000

0

80 82 84 86 88 90 92 94 96 98 00 02 04 06 08

Year * August 2008



five-fold increase in catastrophic climate events caused by floods and destruction by torrential rains and hurricanes over the last ten years. However, the number of deaths caused by such events was close to zero, thanks to disaster risk prevention plans. Despite such increases in extreme events, malaria is at the lowest levels in the history of the country due to the strategic development of a control program. Some isolated outbreaks have been reported in regions free of transmission, originating from migration of workers to tourist areas.

Dengue is not transmitted at home

Dengue is slightly below the incidence patterns, and the most severe forms of the disease observed in Asia in the first 21 years of epidemic hemor-rhagic dengue outbreaks have decreased in most countries, except Thailand. Also dengue hemor-rhagic fever incidence in the Americas shows a clearly rising trend (see Figure 3). However, comparing its behavior in Thailand with the various regions of America indicates that they follow a similar trend (see Figure 4). In other words, it would seem that climate change still does not have an actual impact on the global behavior of dengue in the countries compared.

The outbreaks of dengue in Singapore provide guidelines to help interpret dengue epidemiology. After almost 30 years of very energetic control, major dengue outbreaks occurred, despite indices of positive dengue vectors remaining below or around 1%. The affected age groups included the young and adults, unlike the other Asian countries where the under 15’s have been the most affected age group. It is possible to reach two general hypotheses:

• The dengue trigger threshold does not really depend on a certain vector density, but rather it may depend more on the cumulative number of susceptible people, since there had been no out-breaks for many years; and • as observed by some researchers in Singapore, transmission may not occur within the home.

These two observations can help one understand the problem if considered within the epidemio-logical dynamics of the Americas. Most notified cases and prevalence studies in America show that children from 1 to 4 years of age are not the most affected by hemorrhagic dengue. It would seem rather, that transmission in the home is of second-ary nature, since for 5 to 9 year old children, the older they get, the higher the antibody prevalence

DENGUE HEMORRHAGIC FEVER has been monitored over the first 21 years of epidemic outbreaks originally observed in Asia. Incidence patterns have decreased in most areas, except the Andinean region and particularly Thailand.

Dengue hemorrhagic fever*: first 21 years of transmission* in Thailand, Central America & Mexico, Andinean and Amazone regions

Fig. 4

45,000

40,000

35,000

30,000

25,000

20,000

15,000

10,000

5,000

0

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21

Years of transmission




Article on the enclosed Public Health CD-ROM

Climate change, its origins and consequences, need greater attention from governments and society as a whole. This should focus on the development and launch of public policies that encourage people to use less energy, modify their consumer patterns and preserve the envi-ronment. Effective programs for VBD control will need to be developed in order to prevent their exacerbation and the increase in current trends with their implications and risks for public health.

CONCLUSION

and disease incidence. Furthermore, each time a serotype re-emerges, the number of hemorrhagic dengue cases increases even more. This could be explained by the higher number of previous primary infections. Although dengue epidemiology and transmission dynamics need to be researched further, the implications of these two observations and of the behavior of dengue in Asia since the 1950’s, seem to open up a different explanation for a disease new to the Americas. However, research needs to be based on an older disease for Asia.

Other VBDs in the Americas

Other diseases such as Chagas have been increasing, but so have diagnostic and treatment procedures. Leishmaniasis seems to be stable, with some out-breaks caused by settlements and changes in land use. Onchocercosis has been almost eliminated. Severe leptospirosis has increased as a direct result of flooding, as has severe rickettsias, perhaps due to the increasing sensitivity of epidemiological monitoring systems for hemorrhagic dengue. However, for the Western Nile virus (WNV), there are no records of incidences similar to that in the United States of America. Aedes albopictus increasingly colonizes large areas in the northeast and south border regions of the US and many Latin American countries. Some experts have considered that these latter two events are a result of climate change, and it was expected that they would have a major impact in the other American countries. However, to date neither WNV nor Aedes albopictus seem to have affected much of the American population. It is possible that epidemics may break out in the future. We must not neglect this possibility and we should continue the necessary epidemiological monitoring and efforts to control their vectors permanently.

Recommendations for immediate action

This is a good time in history to test predictive and control models for prevalent diseases that may eventually be modified by climate change. Better control schemes for dengue, for example, do not need to wait for climate change, since we have already been unable to prevent these diseases

globally. Neither should we expect malaria to decrease in the Americas. While in some countries malaria may seem to be a problem that can be eliminated, it might resurge in uncontrollable out-breaks or become a neglected disease.

There is much potential for new diseases such as chikungunya or others to become a threat to the population of the Americas, and changing climatic conditions will provide more ecological options for such diseases to emerge and become estab-lished. This is why we need to insist on a coordi-nated approach to epidemiological knowledge and more efficient vector control in all the countries of the region. There is also a need for greater synchronization of efforts from all the countries to reduce the risk of diseases that are already present. At the same time, preventative measures should be applied for those that may become a threat in the future.

The risks of these diseases need to be managed using other approaches, such as suitable housing improvement. We must remember that hygiene and sanitation models need to be developed that will be affordable for the more marginalized sec-tors of the population. Poverty is not a synonym for health hazards, although this idea seems to persist.



lague is a serious and often fatal illness caused by the bacterium

Yersinia pestis. The disease has been responsible for at least three major pan-demics, affecting millions of people worldwide. The most infamous, known as the Black Death, occurred during the 1400s and decimated a third of the European population.

Today, plague continues to pose a threat to humans in many parts of the world, with 1000-3000 cases being reported by the World Health Organization annually, although many cases may go unreported in remote regions. Current

P

Climate impact on fleas and rodents Implications for future human plague risk in the western United States

Linkages between climate and the spread of plague have been recognized for nearly a century. Local precipitation, temperature, and humidity, and large scale climatic cycles, such as the Pacific Decadal Oscillation, are among the climatic factors that have been found to be associated with the seasonality of plague trans-mission or the occurrences of plague outbreaks in humans and other animals of the western United States.Ph

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foci of infection exist in central and far eastern Asia, India, Africa, the western United States and in South America. The greatest numbers of human cases per year have been reported from Africa in recent decades.

Although more than 200 mammalian species from at least 6 different orders have been reported with Y. pestis infec-tions, the bacterium primarily cycles between rodent hosts and flea vectors. In the mammalian host, the bacterium causes a septicemia, and transmission to fleas occurs during blood-feeding. Within the flea, Y. pestis forms a bio-film, which might facilitate transmis-sion and long-term persistence of the infection in the flea. Recently, a mode of transmission, termed early phase, has been proposed to be important for spread of the disease during epizootics and probably some human epidemics. Although, humans typically become infected by the bite of an infected flea, transmission through direct contact with infected animals or inhalation of infectious materials may also occur.

In North America, plague was first reported in the US in 1899 on ships in many of the country’s ports, including California, Washington, New York, Texas, and Louisiana. Initially, human cases were associated with commensal rats (Rattus spp.) and their fleas. The first confirmation of plague in a wild species was in California ground squirrels (Spermophilus beecheyi) near San Francisco in 1908. Plague is now firmly established in sylvatic (native or wild) rodent communities in the United States, west of the 100th meridian, and causes periodic die-offs of highly sus-ceptible species, including wood rats (Neotoma spp.), ground squirrels (Spermophilus spp.), tree squirrels (Sciurus spp.), chipmunks (Tamias

The authors: ANNA M.

SCHOTTHOEFER, KENNETH L.

GAGE

Centers for Disease Control and

Prevention (CDC);National Center for Zoonotic, Vector-

Borne, and Enteric Diseases; Division of Vector-Borne

Infectious Diseases;Fort Collins, USA

spp., Eutamias spp.), and prairie dogs (Cynomys spp.). In the twenty-five year interval from 1978-2003, an average of about 12 persons per year contracted plague infections in the US. Risks of human infection are linked to living in close proximity to the ecological habi-tats that support sylvatic hosts, and it is generally believed that human cases most frequently occur in association with epizootic events in these hosts.

Relationships between climate and human plague risk

The links between climatic events and plague outbreaks in humans have long been recognized. During the investiga-tions of epidemics in India in the early 1900s, seasonal patterns of rainfall and temperature were described in associa-tion with the occurrence of human cases. In Vietnam, human epidemics were also shown to be influenced by meteorological conditions. In general, cases in these areas were noted to be most frequent in the warm, drier peri-ods following monsoons, but to disap-pear when temperatures exceeded 27°C or saturation deficits exceeded 0.76 cm. Temperature and humidity are known to affect flea survival and activity, and the ability of the flea to transmit plague efficiently many days after becoming infected may be regulated by tempera-ture. Therefore, it was presumed that the declines of human epidemics observed during such hot weather were explained by lower flea abundances and activity, as well as the above-noted impacts of elevated temperatures on the transmission of Y. pestis by fleas.

From retrospective studies conducted in the southwestern US, the frequency of human plague cases appears to be


correlated with two favorable climatic conditions: wet winter-spring months followed by moderate to cool summers. Observations support the trophic cascade hypothesis, which suggests above average rainfall in the winter-spring months of previous plague years promotes vegetation growth, providing more food resources to support popula-tion density increases in rodent hosts. In addition, milder temperatures and humid conditions enhance flea survival and reproduction, and the combination of high rodent and flea populations leads to more plague transmission.

However, the response observed between increased plague activity in humans and the occurrence of wetter periods was mediated by summer tem-peratures. Cool summer temperatures might prolong flea survival and condi-tions favorable for transmission of

Y. pestis by fleas, thereby extending both the duration of epizootic activity and periods of elevated human risk (see figure below).

Similar responses to climate have been documented for plague activity on black-tailed prairie dog (Cynomys ludovicianus) colonies. Plague out-breaks were more likely to occur in prairie dogs in Montana during the years following above average rainfall in the preceding April-July months and with fewer days with maximum daily temperatures exceeding 29.4°C during the concurrent summers.

Across larger geographic scales, recent evidence supports the notion that plague activity in the southwestern states and other regions of the American West is driven by large-scale climatic forces, specifically the Pacific Decadal

HYPOTHESIZED RESPONSES of rodent and flea hosts to climatic variables that lead to increased epizootic plague activity and human infection risk in the western US.

Influence of climatic variables on plague risks

Increased late winter-early spring precipitation

Increased growth of vegetation following rain and snow

More vegetation means more rodent food sources (leaves, fruits, nuts, insects)

Increased rodent densities increase likelihood of epizootic activity

Increased rodent survival

and reproduction (1 or 2 year time

lags)

Increased soil moisture favors flea reproduction

and survival

Increased human plague risks

Warm spring temperatures

Early season warmth favors flea population growth prior to transmission season

Cool summers can prolong epizootics by increasing survival of infected fleas

Widespread epizootics




dance to these events. Further shifts in the rodent community dynamics at this location were observed following two extreme flooding events that occurred in later years, and which have persisted for at least 6 years following the events, demonstrating the potential long-term effects that brief, but severe, climatic events may have on rodent populations. Other studies in plague endemic regions of the American Southwest have found strong numerical responses in deer mice (Peromyscus maniculatus) populations following above average seasonal rain-fall events consistent with that proposed by the trophic cascade hypothesis.

Current evidence suggests that the climatic conditions that favor high rodent densities typically also support high flea densities. Moreover, it was determined that flea species that are competent plague vectors tend to be found at higher densities on their hosts than poor vector species. Thus, environ-mental conditions that positively influence flea abundances will likely also be associated with high plague risk to humans in the future.

Ambient temperature and relative humidity are known to strongly influ-ence flea survival and reproduction. Eggs are vulnerable to low tempera-tures and desiccation. Adult fleas also are generally susceptible to drying con-ditions, although the range of tempera-tures and relative humidities adults of different species can tolerate varies depending on the ecology and environ-mental conditions associated with the activity patterns of their hosts. Larvae of flea species, on the other hand, may be universally susceptible to low and extremely high humidities. Pupae of some flea species, particularly the cat flea (Ctenocephalides felis felis), may be able to survive for extended periods

Oscillation (PDO) and El Niño Southern Oscillation events (ENSO). High num-bers of plague cases simultaneously occurred across the region during posi-tive phases of the PDO, when climate conditions were warmer and wetter. Higher numbers of plague cases were also found to be associated with positive ENSO phases occurring during the pos-itive PDO phase, suggesting the ENSO contributes to the interannual dynamics of plague cycles. The positive associa-tion between warm, wet conditions and plague activity probably relates to the suitability of such conditions for rodent and flea populations.

Relationships between climate and rodent hosts and flea vectors Understanding how changes in climate will affect the spread of plague and its risks to humans in the US will require detailed models. These should accu-rately predict responses by the rodent and flea communities involved in plague maintenance and persistence in the region. In order to produce these models additional long-term data are needed on the effects of climate on rodent and flea population dynamics. Existing data suggests that rodent populations are strongly influenced by climatic variation, although these responses vary among species and locations.

In a non-plague endemic region of the Chihuahuan desert of Arizona, some rodent species declined. For example, populations of the kangaroo rat, Dipodomys spectabilis, and a pocket mouse, Perognathus flavus, responded negatively to vegetational changes that coincided with ENSO events occurring between 1977 and 1992. In contrast, two other pocket mice species (Chaetodipus penicillatus and C. bay-leii) significantly increased in abun-

THIS DOCTOR FROM 1720 is wearing a protective mask and smoking profusely to avoid catching the plague from the air. Plague can be caught by direct contact with animals or inhaling infected materials. However, now we know it is mainly trans-mitted by the bite of a flea living on rodents.




during unfavorable environmental con-ditions if left undisturbed in their cocoons. Unfortunately, responses to changes in temperature and relative humidity have not been well documented for all the life stages of flea species commonly believed to be important plague vectors in North America. This would include many species of ground squirrel and prairie dog fleas that inhabit burrows and might be expected to be somewhat protected from surface-level fluctua-tions in temperature and humidity. However, it should be remembered that those Y. pesitis-infected adult fleas most likely to encounter new hosts after their original ones have died of plague, are those that quest for hosts near the entrances of burrows. These are the ones in a position to leap onto hosts passing by these burrows, and continue the chain of transmission. Unlike fleas

hiding deep in burrows, those at burrow entrances are much more likely to be exposed to the potentially lethal effects of high temperature and low humidity.

Future predictions of climate change and their implications for human plague According to future climate change scenarios, the geographic region cover-ing the current plague foci in the west-ern US will become hotter and drier. Increases in maximum summer tem-peratures are likely, and the frequency of hot days is predicted to increase. Since 1950, the western US has also already experienced a shift in mountain precipitation from snow to rain, earlier snow melt, and changes in river flow because of greenhouse gas emissions. More frequent hydrological extremes, such as droughts and intense precipita-tion events and flooding are expected in the future.

Human plague cases in the US

* rural = > 16.18 ha per housing unit, exurban = 0.68 – 16.18 ha per housing unit, urban-suburban = < 0.68 ha per housing unit

Category *

Rural

Exurban

Urban-Suburban

Total area in 2000

(ha)

52,081,648

2,271,897

5,738,807

Total area (ha)in 2020

(% change)

48,587,419 (-7.2)

3,606,713 (37.0)

988,718 (42.0)

Number of cases

2000-era

26

20

0

Number of 2000-era cases

per unit area (ha)

4.99 × 10-07

8.80 × 10-06

0

Projected number of cases

2020-era

24.26

31.75

0

AREAS AND NUMBERS OF PLAGUE CASES recorded in Colorado, New Mexico, Arizona and Utah between 1996 and 2007 (2000-era) used to predict cases between 2014 and 2026 (2020-era): Rural areas and thus population numbers and plague cases are expected to decrease. Exurban population areas associated with the highest risk are expected to grow, along with the number of infections. Urbanization presents little or no risk of plague infection.

PLAGUE is caused by the bacterium Yersinia pestis.



Because plague outbreaks have been observed to decline during hot, dry periods, a reduction in future plague activity in the US may be expected. It is also possible, however, that plague foci will shift in location, moving northward in latitude and upward in elevation to areas that will retain climatic conditions favorable for continued plague trans-mission.

Human plague risks are associated with living within or near the ecosystems that support competent plague rodent hosts. Our ability to make predictions about future human plague risks will depend on improving our understand-ing of how the intersection of climatic, ecological, and societal changes may be altered. Human populations are expected to grow in the western US, in areas currently associated with high plague risk (see table left). However, heavy urbanization of the landscape is associ-ated with decreased plague risk in humans and prairie dogs. Thus, disentangling the effects of direct human use and climate on habitat mod-ification and the net effects on future plague activity will be a challenge.

We may expect to see more human cases in areas where plague epizootic activity frequently occurs as these areas are converted from rural to semi-rural and lightly suburbanized areas. This is supported by the human plague rates observed in these types of areas during the 2000-era (see table), and by previ-ous investigators. Natural habitats con-tinue to change because of climatic factors and human-related activities, however, fewer cases may be observed in the long-term. Article (with references) and

an additional figure on the enclosed Public Health CD-ROM

In conclusion, current predictions by climatologists sug-gest that conditions in plague-endemic regions are likely to change in ways that will affect the distribution and intensity of human plague risks. In order to address these changes, we suggest that future research programs focus on improving our understanding of:

• flea survival, reproduction, and behavioral responses to fluctuations in temperature and precipitation,• flea vector competencies under different ambient temperatures and humidities, and • how modifying the dynamics of the ecosystem water balance may influence the suitability of habitats for sylvatic rodent hosts, their fleas, and plague transmission.

Key to designing appropriate studies to alleviate these knowledge gaps is a better understanding of how precipitation and temperature regimes are changing in the current plague foci and across the western US. It is also important to know how much they can be expected to change in the future. A deeper understanding of the eco-logical consequences of more extreme intra-annual pre-cipitation patterns also is necessary to be able to make predictions about future human plague risks. Finally, it is important to investigate how climate change interacts with other human-related changes, such as land use modi-fications and demography.

CONCLUSION

MANY DIFFERENT RODENTS are hosts for fleas infected with plague bacteria. Climate conditions that favor high rodent populations usually support high flea densities.

Photo: PureStock


Invaluable for research-ers and policymakers

This fourth report in the IPCC series brings together the latest scientific assessments of climate change by the world’s leading experts.

The IPCC (Intergovernmental Panel on Climate Change) was established by the World Meteorological Organization (WMO) and by the United Nations Environment Programme (UNEP) to provide an objective source of information about climate change.

Apart from a technical summary, it also analyzes in detail the impacts on natural and human environments and their vulnera-bility. A chapter devoted to human health is followed by indi-vidual chapters focusing on a range of issues, including infec-tious diseases, which are specific to particular regions such as Africa, Asia, Europe, Latin and North America.

One message is clear: changes in temperature, humidity and pre-cipitation affect environments for vector-borne diseases, and can create new conditions for disease outbreak. As this report points out, the populations that might be particularly affected are those at the boundaries of current disease areas. The report also includes a CD-ROM with a range of supporting material, with a data-base of references and figures in Powerpoint – ideal for anyone preparing presentations on the subject. This book will be an invaluable source of information for a wide range of researchers, organizations and NGOs. In fact, anyone looking for concrete data on the multiple and complex issue of global climate change will find it interesting.

Climate Change 2007 – Impacts, Adaptation and

Vulnerability Contribution of Working Group II to the Fourth Assessment Report of

the Intergovernmental Panel on Climate Change

(Cambridge University Press, 2008)

Facing the threat of old and new diseases in Europe

The 24 chapters in this book are from different authors, all recog-nized experts in their different fields – some have also contrib-uted articles to this current Public Health Journal. The book’s over-all theme is the already observed and anticipated further increase in vector-borne diseases and pests in Europe, whether due to climate change or other factors.

In the past, pests and vector-borne diseases such as the plague, malaria and yellow fever were

Emerging Pests and Vector-Borne Diseases in Europe

(Ecology and Control of Vector-Borne Diseases: Volume 1)

by Willem Takken (Editor), Bart G.J. Knols (Editor), (Wageningen Academic Publishers, 2007)

common in Europe. Improved hygiene, sanitation, drugs and medical treatment, as well as measures to control disease-carrying vectors and pests elimi-nated most of these diseases from Europe several generations ago. But these diseases still cause suffering and death in many

N O T E S

A great number of books have been

published on the general theme of climate change,

as well as how this may affect public health. We

have chosen the following books for the range of

up-to-date information. These also highlight

different ways of considering the challenge of

climate change.


warmer countries worldwide. Today, in addition to climate change, globalization with increased trade and travel mean much greater movement of people and animals, including uninten-tional insects or pathogens. This causes concerns that not only some of these diseases might return, but also diseases and pests new to temperate regions could spread to Europe. Chikungunya outbreaks moving to northern Italy (see Public Health No. 19, page 56) provide a worrying example.

The authors describe the most likely vector-borne diseases and pests posing a threat to humans and animals in Europe. Understanding the ecological factors that favor such pest and vector proliferation, and imple-menting effective surveillance systems for their early detection will be essential for the inter-vention and prevention of these

Challenges facing the health sector

The success of pathogens and vectors is partly determined by their reproduction rates: increases in temperature reduce the time needed to breed. This in turn affects disease transmission, an important theme when con-sidering the effects of climate on human health. Here, the WHO, the World Meteorological Organization and the United Nations Environment Programme have combined forces to produce this book focusing on the chal-

lenges facing the public health sector due to global climate change.

Indeed, the effects of climate on the transmission biology of infec-tious diseases are best illustrated by vector-borne diseases. This includes the complexities of interactions between the environ-ment and disease hosts. A recent example is many tropical islands reporting outbreaks of vector-borne infectious diseases partially due to changes in temperature and rainfall.

A further aspect is the impact of climate extremes, such as El Niño on health and the spread of vector-borne diseases such as dengue fever. One vital question raised by this book is hard to answer: “How much disease could climate change cause?”

Climate Change and Human Health: Risks and Responses

by D.H. Campbell-Lendrum, C.F. Corvalan, Kristie L. Ebi,

A. J. McMichael (World Health Organization, 2003)

Forecasting disease epidemics

It has long been known that changes in weather conditions are linked to the emergence of infectious diseases. The question is, can we use modern climate

Under the Weather: Climate, Ecosystems and Infectious

Diseaseby Ecosystems, Infectious Diseases, and Human Health Committee on Climate, Board on Atmospheric

Sciences & Climate, the National Research Council

(National Academy Press, 2001)

and weather forecasting to pre-dict the outbreak and transmis-sion of epidemic diseases? Or more importantly, to predict how global warming will affect the spread of these diseases world-wide?

“Under the Weather” analyzes links between climate, ecosys-tems and infectious diseases. It also describes the directions scientific research should take to better understand these extremely complex interactions. The goal is to potentially transform weather and climate forecasting into a tool for public health. This will help policymakers, organizations and governments to predict and prevent outbreaks of disease. By incorporating what we have already learned from using climate forecasts in other human activities, such a tool could be used as an early warning system for epidemics.

B O O K R E V I E W


Since children and young people are not only curi-

ous and open to new ideas, but also the key to the future, Bayer Environmental Science has helped develop various educa-tion tools especially designed for them. Taking the form of comic strips and a soundbook, these are ideal for schools, dis-pensaries and clinics, and for both children and adults.

Children in Africa bear a heavy burden with malaria. At the same time, these young people represent a large and enthusiastic section of the population ready to learn about the disease and its prevention.

For children of all ages!

Educational tools

The K-O Kid

The comic series “Adventures of the K-O Kid” is part of the Bayer Kick Out Malaria Initiative to treat bednets in the field with K-O Tab® 1-2-3. This product converts the nets into longer-lasting insecticide-treated mos-

quito nets (see PHJ No. 17). In super hero cartoon style the K-O Kid’s mission is to protect those at risk (e.g. pregnant women and young children) from the evil biting mosquitoes. The K-O Kid does this in various adventures telling stories about proper use of bednets.


Comic strips explain what malaria is, its symptoms, how it is caught and the impor-tance of sleeping under treated bednets in simple to under-stand words and pictures. Bayer Environmental Science develops and supports educa-tion tools designed especially for children and young people. By addressing the children, this also reaches their parents.

CONCLUSION

Talking book

The “Moving against Malaria” soundbook is the result of cooperation between Malaria No More, Department of Health of South Africa, World Vision, Bayer, BASF, USAID, NetMark, and AED. Fascinating for the smallest children and even adults, you don’t even need to read it. By pressing the symbol in the right hand panel corresponding to the one shown on each page, Yvonne Chaka Chaka speaks the text above the picture. With simple words and pictures, the book describes malaria, its symptoms, how one catches it, getting treatment, and how to keep safe from the disease by sleeping under a treated bednet.

Cartoons can instruct

CHEPE/Carole Productions* concentrate on cartoons to pro-vide easy to understand informa-tion and advice about various health themes. Doctors and nurs-es help the graphic designers and story writers develop the story. Each one explains a disease, its symptoms, treatment and ways to prevent catching the disease. These are published in a number of different European and African languages. The African cartoons

feature the hero Juma, a young boy who faces a different dis-ease or problem (e.g. schistoso-miasis or vaccinations) in each colorful booklet. In a joint production with Bayer Environmental Science, Juma helps the reader to learn all about malaria, why it is important to use treated bednets and how to treat them in the field. This is not just informative for children, but also serves as an instruction booklet for adults who cannot read properly.

M A L A R I A

* in close cooperation with ministries of health, international organizations (WHO, UNICEF, UNAIDS), international NGOs, local networks and the private sector. [email protected]

N O T E S


Bluetongue: Spreading north Surviving another winter in Northern Europe, the first cases of bluetongue in 2008 began to appear in July. Most cases reported in France were located along the front line of last year’s outbreaks. This suggests the biting midges that transmit the disease are spreading north.

Bluetongue is a disease of ruminants and vacci-nation against this vector-borne disease is com-pulsory in France. However, it is voluntary in England, with farmers starting to vaccinate live-stock last year when bluetongue arrived in the south-east. This summer the race to protect live-

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stock at risk moved the vaccination “front” up to Yorkshire in northern England.

Northern regions of Britain are the country’s main sheep areas, and while bluetongue makes cows ill, it kills sheep. This means sheep just outside the vaccinated zone are at high risk of contact with infected livestock. Subsequent spread of the virus depends on whether enough livestock have been vaccinated south of the line to slow down transmission of the disease.

Source: New Scientist

By 2007, about 19% of African children living in areas where malaria was endemic were sleeping under insecticide-treated mosquito nets, according to a new study in the Lancet. In 2000, fewer than 2% of African children had them. But even though coverage has increased sharply, mainly due to free distribution of nets, 90 million children are still unprotected. More than half of these missed

Malaria nets: millions of children still unprotected

children were in just seven countries. Some countries did particularly well; Eritrea reached 85% coverage. But Nigeria, Uganda, Mozambique, Ivory Coast, Cameroon, the Democratic Republic of Congo and Sudan – the last two of which are at war – were below 15%.

Source: New York Times

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N O T E S

Bayer has already been recog-nized internationally as “best-in-class” in climate protection and as a leading company in its sector. In production, it has been able to increase energy efficiency in recent years through techno-logical innovations and has significantly reduced greenhouse gas emissions. In addition, Bayer products make a direct contribu-tion to saving energy and conserving resources in our daily lives, for example in the form of insulating materials.

Bayer intends to intensify its efforts even further. It will use its innovative capabilities and know-how as an inventor com-pany to develop new products and solutions for climate protec-tion and for dealing with climate change. It has therefore set ambi-tious new targets for reducing greenhouse gas emissions between 2005 and 2020. For example, the Bayer MaterialScience subgroup aims to cut its worldwide specific CO2 emissions for every metric ton of products it sells by 25%. Absolute emissions from the less energy-intensive subgroups, Bayer CropScience and Bayer HealthCare are to be cut by 15% and 5%, respectively. Bayer will also invest Euro 1 billion in climate-related R&D and projects until 2010.

Our planet – the only one we haveAs a socially responsible company, Bayer is committed to playing an active role in overcoming one of the biggest challenges of our time. For this reason, the company initiated at the end of 2007 the group-wide “Bayer Climate Program”, which is designed to run for several years.

Bayer Climate Program

Lighthouse projects

The Bayer Climate Program has already initiated several light-house projects, which provide groundbreaking examples of initiatives aimed at tackling the consequences of climate change and supporting climate protec-tion. Bayer EcoCommercial Building is a concept for zero-emission office and industrial buildings that can be built in all

the Earth’s climate zones. Stress-tolerant plants can deliver good yields even under extreme con-ditions such as heat and drought. Biofuels, i.e. plant-based fuels cut emissions and help ease pres-sure on resources. Bayer Climate Check focuses on production processes and investment projects.

Further information: www.climate.bayer.com

International Children‘s Painting Competition

How do children perceive climate change? The answer to this question can be seen in the International Children‘s Painting Competition 2007, run as part of a partnership between the United Nations Environment Programme (UNEP) and Bayer AG. The pictures were submitted by 13,500 children from 104 countries. Their joint message to the whole of humanity is: Take care of our endangered planet, because it‘s the only one we have! On behalf of Bayer, pho-tographer Peter Ginter visited eight children in their home countries. He photographed them – together with their works – in their natural environment. At once expressive, pointed and alarming, these photos illustrate how the children are depicting a very accurate image of our world.

A selection of the winning pictures can be seen at:www.climate.bayer.com/en/seeing-the-world-through-childrens-eyes.aspx

Lakshmi Shree (10 years), India



R E T R O S P E C T I V E

t was not until 1981 that the entomologist Willy Burgdorfer

managed to isolate a spirochete bacterium, later named Borrelia burgdorferi (Bb) after him. Born and educated in Basel, Switzerland, Willy Burgdorfer was familiar with European medical publications. Burgdorfer,

Jorge Benach and Edward Bosler exam-ined black-legged (deer) ticks for patho-gens. Finally, they observed a poorly stained, spiral-formed bacteria in tick body

fluid, and then in patients with Lyme disease. These spirochetes proved to be the major disease-causing agent of Lyme disease.

Multiple linked symptoms

As early as 1883, a skin condi-tion now associated with Lyme disease was first described by the physician Alfred Buchwald in Wroclaw, Poland (then Breslau, Germany). Later, Arvid Afzelius reported his work on a ring-like skin rash at a Swedish Society of Dermatology meeting in 1909. His published results implicated the bite of an Ixodes tick as being responsible for the circular rash

History: Lyme disease

Physicians in Europe have described symptoms associated with Lyme disease for over 100 years. Correctly speculated as transmitted by the bite of a tick in the early 1900s, treatments with antibiotics in the 1950s pointed to a bacterial pathogen. But it was not until 1976 that a misdiagnosis of juvenile rheumatoid arthritis first gave the disease its popular name.

now known as Erythema migrans (EM). Subsequently, many other physicians observed EM associ-ated with flu-like symptoms. Sometimes this was followed by arthritic joint pains, neurological problems, psychiatric symptoms, benign lymphocytomas and cardiac problems.

Antibiotic clue

In the 1920s French physicians Garin and Bujadoux postulated that various symptoms following a tick bite were caused by a spirochetal infection. Swedish dermatologist Carl Lennhoff observed spirochete structures in skin samples in 1948. This inspired experiments with penicillin in the 1950s, which showed success in treating these conditions. Confirming that

bacteria cause this disease, treatment today is based on a range of tetracycline or penicillin-derived antibiotics.

Reaching the USA

In 1970, Rudolph Scrimenti diagnosed the first case of EM in the US and based on European results, treated the tick-bitten patient with penicillin. Researchers in Connecticut identified clusters of an arthritic disease in 1975, including cases in the towns of Lyme and Old Lyme. This is why Allen Steere and colleagues called this condition “Lyme arthritis”.

When US patients with Lyme arthritis were also discovered to have EM, this condition was recognized as being the same tick-borne disease found in Europe. Since 1976 the disease is usually called Lyme disease, Lyme borreliosis or just borrelio-sis. It is now the most common tick-borne disease of North America and Europe – and the number of cases and endemic regions are increasing.

I

More

www.lyme.org

LYME DISEASE is named after a town in Connecticut.

Willy Burgdorfer

PUBLIC HEALTH JOURNAL: No. 20 on CD-ROM

We wish you a pleasant and informative read.

If the CD-ROM is missing, please contact your Bayer Environmental Science regional manager for a complimentary replacement (see green box on the right).



Bayer Climate Programwww.climate.bayer.com

Bill & Melinda Gates Foundationwww.gatesfoundation.org

CDC (Centers for Disease Control and Prevention)www.cdc.gov

Colorado State Universitywww.colostate.edu

CORE Groupwww.coregroup.org

GBC (Global Business Coalition)http://www.businessfightsaids.org

Global Fund to Fight AIDS, Tuberculosis and Malariawww.theglobalfund.org

IPCC (Intergovernmental Panel on Climate Change)www.ipcc.ch

IRAC (Insecticide Resistance Action Committee)www.irac-online.org

LSHTM (London School of Hygiene and Tropical Medicine)www.lshtm.ac.uk

LSTM (Liverpool School of Tropical Medicine)www.liv.ac.uk/lstm

Medical University of Vienna www.meduniwien.ac.at

Millennium Development Goalswww.undp.org/mdg/basics.shtml

PSI (Population Services International)www.psi.org

RBM (Roll Back Malaria Partnership)www.rollbackmalaria.org

UNEP (United Nations Environment Programme)www.unep.org

UNICEFwww.unicef.org

University of Oxford www.ox.ac.uk

USAIDwww.usaid.gov

Wageningen University www.wageningenuniversiteit.nl/uk

WHOwww.who.int

WHO (Neglected diseases)www.who.int/neglected_diseases/

World Bankwww.worldbank.org

Link ListWith reference to the topics in this issue of Public Health Journal we include a summary of the main Internet links, where you can find further information, the latest reports and statements.

Business Manager Vector ControlGerhard Hesseemail: [email protected]

Australia / PacificJustin McBeathemail: [email protected]

CARTSEEBora Erbaturemail: [email protected]

India Anil Makkapatiemail: [email protected]

Latin AmericaClaudio Teixeiraemail: [email protected]

MENAPAshraf Sheblemail: [email protected]

Southeast AsiaJason Nashemail: [email protected]

Sub-Saharan AfricaMark Edwardesemail: [email protected]

Events5th European Mosquito Control Association WorkshopMarch 9 – 13, 2009 Turin, Italy www.zanzare.eu

12th World Congress on Public Health April 27 - May 1, 2009Istanbul, Turkeywww.worldpublichealth2009.org

5th MIM Pan-African Malaria ConferenceNovember 2-6, 2009 Nairobi, Kenyawww.mimalaria.org/pamc/


FOR INFORMATION PLEASE CONTACT

You can find all links on the enclosed Public Health CD-ROM

PUBLIC HEALTH JOURNAL: No. 20 on CD-ROM

As a special service for readers of Public Health Journal we include a CD-ROM (see inside back cover). Not only does it contain every page of the complete issue in pdf format, but also the individual articles. Some feature additional information.

Imprint

Public Health Bayer Environmental Science Journal No. 20February 2009Publisher: Bayer Environmental Science SAS16 rue Jean-Marie Leclair CP 106, 69266 Lyon Cedex 09, FranceEditor-in-charge: Gerhard Hesse email: [email protected]

Editors: Michelle Cornu, David Coop(Bayer Environmental Science), Michael Böckler (SMP Munich), Avril Arthur-Goettig Realization: SMP MunichLayout: Artwork (Munich)Printing: Mayr Miesbach GmbH (Germany)

Comments expressed in this Journal are the views of the authors, not necessarily those of the publisher. Copying of any text and graphics is only allowed with permission of the publisher and/or specific author(s) of the relevant article(s).


T W O D E C A D E S O F P U B L I C H E A LT H J O U R N A L Over 20 years, Bayer has been publishing the Public Health Journal to provide information on pest-related health issues with special emphasis on vector-borne diseases, its sustain-able and effective control and the environment of stakeholders. Times have changed, and

so has the journal, but the themes addressed are more up to date than ever.

A Business Operation of Bayer CropScience

PHJ_20_Complete_Issue

Documents

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