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CSIRO Entomology, Indooroopilly, Queensland, Australia 4068
SUMMARY INTRODUCTION SCENARIOS OF GLOBAL CHANGE Atmospheric Composition Climate Change Climate variability and extremes. Analogues of climate change. Urbanization Land Use, Land Cover, and Biodiversity Industrial and Agricultural Pollution with Hormone-Disrupting Chemicals Trade and Travel FRAMEWORK FOR ASSESSMENT OF IMPACTS TO VECTOR-BORNE DISEASES UNDER GLOBAL CHANGE Exposure Sensitivity Impacts Benchmarks for Measuring Impacts IMPACTS Atmospheric Composition Climate Change Malaria (i) Exposure and sensitivity (ii) Extreme climatic events and malaria transmission. Vector-borne diseases other than malaria. (i) Exposure and sensitivity. (ii) Extreme climatic events and vector-borne diseases other than malaria. Urbanization Land Use, Land Cover, and Biodiversity Endocrine Hormone Disruptors Trade and Travel Interactive Effects of Global Change Drivers Summary of Potential Impacts on Key Vector-Borne Diseases FRAMEWORK FOR DESIGNING ADAPTATION OPTIONS UNDER GLOBAL CHANGE ADAPTATION OPTIONS Legislative Engineering and Behavioral Management of vector-borne diseases by vector control. Management of vector-borne diseases by targeting the pathogens. (i) Chemotherapy. (ii) Vaccines. Adaptation of Control Measures for Vector-Borne Diseases in Response to Global Change Adaptation to invasions by exotic vectors and pathogens. Threats to Sustainability of Adaptation Options Resistance. Human safety and nontarget effects of vector control. Community health and public health infrastructure. Adaptive capacity of different social groups. FRAMEWORK FOR ASSESSMENT OF VULNERABILITY CONCLUSIONS ACKNOWLEDGMENTS REFERENCES
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| INTRODUCTION |
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There have been a number of recent reviews covering aspects of global change and human health, including infectious diseases (53, 61, 117, 126, 134, 205, 206, 222, 223, 246, 249). Several reviews have specifically targeted vector-borne diseases (121, 125, 249, 270, 303, 304, 307, 318). There have not yet been thorough quantitative studies addressing the many processes at work (53, 210, 211, 248, 304, 309, 310). In part this is because of the complexity of the many indirect and feedback mechanisms that bear on all aspects of global change. Any consideration of one particular cause of change cannot be made in isolation because of the many interactions between the different drivers of change. As a result, appeals have been made to take a holistic approach to risk assessment and management of vector-borne diseases (117, 121, 208, 220, 268, 307, 347). Unfortunately, the state of current analytical skills and data and the limited resources of the scientific community have resulted in consideration of isolated subsets of those changes in any quantitative risk assessment.
This review focuses on developing a holistic approach to the assessment of vulnerability of societies to vector-borne diseases. The aim is to assess the risks of potential changes in the status of vector-borne diseases in a changing world and to consider approaches to effective adaptation to those changes. The review presents a framework for an integrated assessment of the impacts of different global change drivers and their interactions on vector-borne diseases. The framework enables potentially important secondary interactions or mechanisms and important research gaps to be identified and provides a means of integrating targeted research from a variety of disciplines into an enhanced understanding of the whole system.
The ecology and epidemiology of vector-borne diseases can be described using the "disease triangle" of host-pathogen-environment originally developed by plant pathologists. The disease triangle concept was extended (305-307) to emphasize the role of management in adapting to risks from invasive species and animal parasites. The risk assessment community's concept of vulnerability, as used by the Intergovernmental Panel on Climate Change (IPCC) (244), and the quarantine community's concept of pest risk analysis (146) were included. Here this combined approach is used to structure review material on vector-borne diseases of humans (Fig. 1).
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| SCENARIOS OF GLOBAL CHANGE |
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This giant undesigned and untestable human experiment with the Earth's climate and atmosphere (it is the only one that we have) has already increased the atmospheric concentration of CO2 by almost one-third (Fig. 3a) and doubled the concentration of methane in the atmosphere (Fig. 3b). None of these changes in atmospheric composition is known to affect vector-borne diseases directly. However, the effects of higher concentrations of CO2 on plants are to reduce their water loss through transpiration and to act as a fertilizer. The result is that plants produce more foliage with the same amount of water (261), provided that they do not exhaust the supply of other nutrients. Two consequences of this phenomenon that are relevant to the current consideration of the effects on vector-borne diseases are that the increased density of plant foliage will provide more favorable microclimates for insect vectors and that plant growth seasons will be extended in some situations, effectively increasing the duration of favorable microclimates each year. A further consequence in some habitats may be a larger residual amount of water being left in the soil after maturation of a crop. This could affect water tables and the speed with which soils saturate and produce surface water reservoirs suitable for breeding of mosquitoes. It follows that the increased water use efficiency of plants at high CO2 concentrations may result in an expansion of the ranges of woodlands into lower rainfall areas with adequate soil nutrients, leading to spatial changes in the ranges of vectors in response to habitat changes (95).
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These projected changes rely on extrapolation of expected trends and do not consider possible triggers that may be set off as the Earth's atmosphere warms. One phenomenon that could have overwhelming effects is a failure of the circulation of warm water from the Gulf Stream into the North Atlantic Current, which forms part of a global salt conveyer belt. The current is driven by cold, saline water sinking in giant underwater waterfalls off Labrador and Greenland, which flush the cold water back into the warm Atlantic. Global warming could cause a failure in the flushing mechanism by diluting the saline water with bursting of ice dams from melting glaciers, by increasing rainfall in the region, or by reducing the temperature gradients in the sea. In the past, this has triggered very large (up to 10°C) and very rapid (a decade or century) "flips" in climate every few thousand years, with equally rapid reversals or "flops," leading Calvin (52) to call them climate "flip-flops." The effect is to put the world into a cold-dry climate, with Europe's climate equating to present-day Siberia, with devastating consequences in terms of food supplies for the world as a whole. This would reduce risks of almost all vector-borne diseases, except perhaps flea-borne diseases, among a starving population. An equally rapid warming event would have catastrophic implications for vector-borne diseases, with rapid geographical expansion of tropical ranges affecting nonimmune populations. Since any sudden cooling will greatly reduce the risks of vector-borne diseases and a subsequent warming would be well beyond the time horizon that is relevant to the present topic, these flip-flops are noted for their wider risks but are not considered in this review.
Projected changes in rainfall are even more uncertain than those for temperature, with large differences in the climate projections from different global climate models (GCMs). The consensus is that most tropical areas, particularly over oceans, will receive more rainfall, with decreases in most of the subtropics and relatively smaller increases in high latitudes (144). The uncertainty about rainfall is increased by the potential for geographical and seasonal shifts in rainfall patterns, so that local outcomes are difficult to foresee. Readers are cautioned to interpret the following projections of changes in the status of vector-borne diseases with climate change with care. They are indicative only and are intended to alert the community to some of the steps that can be taken to insure against any deterioration in public health caused by vector-borne diseases.
There have been numerous reports of physical and biological changes in the environment that are consistent with current warming of the Earth's surface. These include an increase in the altitude of the freezing point in the tropics by 110 m (83) and the melting of tropical glaciers around the world (321). A wide range of biological effects of recent climate change has been noted (142, 219, 243, 282), including population and life history changes, shifts in geographical ranges, changes in species composition in communities, and changes in the structure and functioning of ecosystems. In contrast to the tropical effects noted above, increases in the altitudinal range of five species of trees by 120 to 375 m, together with an increase in the tree limit by 100 to 150 m, have been noted at high latitudes in the Swedish Scandes (170). Such widespread biological changes were noted by Epstein (89), who cited them in support of the notion that recent climate change could have contributed to some current changes in patterns of vector-borne diseases. The difficulty faced by researchers is how to separate such effects from the many other simultaneous influences that are usually involved.
Climate variability and extremes. While the primary effect of global warming will be to increase the average temperature of the Earth, the features of climate change that deserve most attention in the context of vector-borne diseases are possible changes in the frequency and severity of extreme weather events and in climatic variability. Even if the variability of the climate relative to the average remains the same, there will be disproportionate changes in the frequency of extreme events, such as fewer frosts and more floods (346), that can have large effects on disease vectors. Of further concern is the fact that the frequency of two successive extreme events is even more sensitive to small changes in the mean. The increasing temperatures will also intensify the hydrological (rainfall and evaporation) cycle (251), leading to an increased frequency and intensity of extreme weather events such as storms, floods, and droughts. Empirical evidence for such a trend is evident in a pattern of steadily increasing proportions of higher rainfall events in the United States (144).
The assumption that the variability of the climate will not change does not appear to hold (154), and it is expected that more cloud cover will increase minimum temperatures and lower the rate of increase of maximum temperatures. The result is likely to be fewer frosts and more moderate increases in the frequency of suboptimal maximum temperatures.
Analogues of climate change. Since the effects of climate change are difficult to study, analogues have been sought to explore the likely consequences of increases in temperature or changes in rainfall (112). They have included historical climates that show insect distributions tracking climate change (63) and different geographical locations, with the expected higher temperatures, for vectors (264). The most popular analogue is the El Niño phase of the El Niño southern oscillation (ENSO) cycle to simulate the effect of global warming. In the absence of the opportunity to observe the effect of climate change over a short period, the temporary, regional warming events associated with the ENSO cycle form an attractive analogue for climate change (37, 127). It is acknowledged that global warming is likely to lead to different combinations of changes in temperature and moisture compared with the ENSO cycle. Nevertheless, some interesting correlations have been made on the incidence of vector-borne diseases in relation to the ENSO cycle.
The ENSO has effects that are felt around the globe (112). El Niño is often associated with heat waves and drought in southern Africa and Southeast Asia including Australia, while it brings floods to the west coast of South America and to central Africa. The opposite phase, La Niña, reverses these patterns. However, enthusiasm for the use of the ENSO may have arisen during a period when the correlation of the index with summer rainfall in northeastern Australia (for example) was particularly high (Fig. 4) (51). The reliability of the ENSO as a surrogate for climate change or as a predictive tool must be questioned in the light of the large, decade-long fluctuations in the relationship. Since the ENSO cycle plays such a dominant role in causing seasonal changes in climate, there is concern that any interaction between anthropogenic climate change and the mechanisms driving the ENSO could have unpredictable results. Unfortunately, there is already a suggestion that the severity of the ENSO cycle may be increasing, with the 1997 to 1998 event being the strongest on record (75), and it occurred simultaneously with an accelerated period of global warming since the 1970s (144).
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Drainage and water supplies are critical factors that determine the extent to which many diseases are either contained or propagate in urban communities. Poverty associated with rapid population growth leads to concentrations of people without the necessary infrastructure for the safe storage and distribution of water and drainage of wastewater. Used containers and tires provide breeding sites for mosquito vectors. In addition, the deteriorating public health infrastructure in many countries exacerbates the health problems (121). Each of these negative societal trends is expected to continue, and water-related issues in particular are expected to increase in importance in the developing world over the next few decades (352). On the other hand, in wealthy communities there is encroachment of residential or recreational populations into forested areas where natural hosts and vectors of vector-borne diseases exist.
Future land cover change will occur mostly in the tropics and subtropics. It is likely to result in increases in surface temperatures of up to 2°C, with drier conditions where the land cover is reduced. In contrast to the reduced diurnal temperature range expected with greenhouse warming, future land cover change in the tropics may increase the temperature range by decreasing evaporative cooling during the day. The sensitivity of surface temperatures to future anthropogenic land cover change in the tropics is up to 1.5°C warmer than the range induced by decadal-scale interannual variability in vegetation density (80).
With changes in land use comes fragmentation of habitats, loss of biodiversity and alteration of existing vector-host-parasite relationships. The rate of species loss is now higher than at any time since the period when the dinosaurs went extinct (175). Fragmentation of habitats isolates populations with low mobility but still provides access to mobile species, thus altering the species balance in undisturbed areas. This can lead to changes in the physical environment for vectors and hence affect patterns of disease.
There were more than 14.5 million refugees worldwide at the end of 2000, 1 million more than 2 years previously (Fig. 5). From the perspective of vector-borne diseases, the most significant problems are likely to occur in Africa, with more than 3.3 million refugees, South and Central Asia, with 2.6 million, East Asia and the Pacific, with 0.8 million, and the Americas, with 0.6 million (13). In addition, a similar number of people were internally displaced within countries, usually from rural areas into cities.
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International trade in merchandise has increased three- to fourfold over the period from 1980 to 2000, with most of the increase occurring in Asia, where there was a fivefold increase in the value of exports (World Trade Organization, http://www.wto.org/english/res_e/statis_e/webpub_e.xls) (Fig. 6). Inevitably, this must lead to an increase in the incidence of vectors being transported to other countries.
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| FRAMEWORK FOR ASSESSMENT OF IMPACTS TO VECTOR-BORNE DISEASES UNDER GLOBAL CHANGE |
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To develop a holistic approach to risk assessment of vector-borne diseases under global change, we need to combine the approaches developed by the different research and policy communities into a comprehensive risk assessment framework. In this review, each of these approaches is called upon to address particular issues.
The concept of vulnerability is useful for assessing risks to human societies from vector-borne diseases. It is used in the scientific and policy communities investigating the likely threats from climate change (140, 144). Vulnerability is a measure of the potential impacts of a given change, taking into account the adaptive capacity that is available to the affected system or community to respond to that change. In other words, it describes the sensitivity of the particular system of interest to vector-borne diseases, taking its adaptive capacity into account (348). The term avoids the misleading practice of considering risks in the absence of a societal response, which can give an exaggerated picture of the perceived risks. In the present context, impacts are a combination of a change in exposure of humans to pathogens with environmental change and the sensitivity of the population to that change. Adaptive capacity consists of the adaptation technologies and cultural tools and the public health infrastructure and resources that are available to implement appropriate management responses. Inclusion of a given society's capacity to implement appropriate adaptive measures discriminates between groups with disparate cultural, economic, or environmental resources that are needed to implement those measures. It helps to highlight those communities, mostly in the developing world, that are not equipped to manage the changes. The relationships of impacts, adaptation and vulnerability are shown below:
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At the global level, assessment of the risks associated with different sources, pathways, and destinations of vectors and pathogens can be assessed by following the quarantine procedures that operate under international "pest risk analysis" agreements for plant health (146). Linking of global change risk assessment approaches with those used by the quarantine community has been proposed (18, 305). The procedure attempts to identify and manage risks by targeting weaknesses at the source of an infection, along the transport pathway and at the destination (Fig. 7). We will see below, when considering adaptation options, that it is more difficult to manage risks when humans are the host of a vector-borne disease than when plants or animals are involved.
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Before proceeding further, it is also necessary to appreciate the nonlinear nature of many biological responses to changes in the environment. These arise from a number of features of biological systems, including thresholds such as developmental or behavioral temperature thresholds, discontinuities at the edges of the ranges of species, nonlinear responses to temperature and moisture, multiplicative effects of population growth in vectors with multiple generations each year, negative feedback associated with competition or predation as population densities increase, interactions between variables resulting in nonadditive effects, and the disproportionate effects of changes in the frequency of extreme events with small changes in the value of the mean. Awareness of such nonlinear effects helps to prevent surprises and so leads to more sustainable adaptation to global change. One consequence of these behaviors is the need to augment empirical and descriptive approaches, such as statistical models, with mechanistic computer simulation models (307).
The sensitivity of a human population to a given disease under global change depends on the combined responses of the pathogen, vector, and host populations. This combination has the potential to generate significant complexity. The geographical location is also a key determinant of the sensitivity of a species to environmental change. A change in the suitability of the environment within the current geographical distribution of the disease will alter the development, survival, and reproductive rates of vectors and pathogens and so affect the intensity of disease transmission and resultant exposure of the population to the disease. The extent to which the exposure changes, following a new introduction of a vector or pathogen or a change in the density of an endemic vector with climate change, depends on the position of the particular habitat relative to the potential geographical distribution of the vector or pathogen in relation to climate (Fig. 8).
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Recognition of variation in the susceptibility of humans to vector-borne diseases, based either on genetic (e.g., sickle cells and malaria) or acquired immunity developed in response to exposure, is needed. The concept of herd immunity leading to endemic stability of a disease is crucial to understanding the dynamics of diseases, the likely susceptibility of populations to such diseases, and the likely consequences of interventions to reduce transmission rates (296). Since the nature of clinical symptoms differs with different transmission rates, it is essential to understand the relationships between pathogen infection, morbidity, and disease outcomes in order to plan interventions that avoid undesirable consequences. These relationships vary greatly with different pathogens, and so a case-by-case approach is necessary.
The sensitivity of a human population to a change in exposure depends on the immune status of the population. Diseases affect human health most severely when there is initial contact resulting from humans entering new habitats, from a spread of disease organisms and their vectors, or from temporary surges in transmission rates during abnormal seasonal conditions, for example. In such cases, naive, nonimmune populations are especially susceptible to epidemics of acute disease.
The rate of disease transmission leads to different disease patterns, such as that for pathogens to which humans can acquire immunity, like malaria (Fig. 9). On a spatial scale, the graph represents a cross-section of Fig. 8. At high transmission rates, a condition known as endemic stability is created, whereby most hosts are immune, creating herd immunity (C). Around the edges of the area of endemicity there are areas with intermittent epidemics of disease (B), which are referred to as endemically unstable areas. These frequently cause the greatest concern because they involve nonimmune hosts that are particularly susceptible to infection in a high-risk environment. The disease is absent from areas (A) that do not provide suitable environmental or socioeconomic conditions for transmission. These areas may be too cold or too dry for the pathogen or vector to develop and survive during the unfavorable season, or they may have human living conditions, such as insect screens or air conditioning, that prevent contact with the vectors. In areas with very high transmission rates, the hosts may succumb to acute forms of the disease if their health is in any way impeded, creating an "overload" condition (D). In the case of dengue, subsequent infection with a different serotype greatly increases this latter risk by causing additional clinical effects with hemorrhagic symptoms (153).
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Climate change and trade and transport in particular have the potential to affect the geographical distribution of vectors. While climate change alters the immediate environment of a vector, translocation to a new region presents similar and probably greater changes for vectors. Such changes need to be studied by using geographical-scale approaches. Sutherst (305) presented a conceptual framework for studying the effects of climate on the distribution and abundance of species and how they are affected by climate. As shown in Fig. 8, populations respond differently to a given change in a climatic variable depending on where they are situated in relation to their climatic envelope.
Integrated assessment frameworks to bring some of these elements together are under development (53, 205, 248) but do not yet incorporate local environmental circumstances (220). A framework for analyzing impacts on parasites has been described (307) based on theoretical ecology and the framework outlined above. The adoption of political ecology as a framework for analysis of emerging infectious diseases has also been advocated (217). The discipline incorporates social, economic, environmental, and biological components to present a holistic approach. Each of these approaches needs a set of analytical tools.
Tools for risk assessment under global change have been reviewed elsewhere (220, 312). A wide range of approaches have been applied to the assessment of risks for humans to vector-borne diseases under global change. They have ranged from the use of historical analogues (121, 267, 269, 270), and geographical analogues (264) to a variety of statistical (193, 194, 280) and modeling (189, 205, 210, 212, 248, 304, 307, 312, 315) tool and models combined with fuzzy logic or rules (68). Historical events are helpful in providing pointers to potential causes of changes in status of diseases (269) but usually suffer from a lack of firm data, sometimes leading to uncertainty in interpretation.
Each technique has limitations, but the most important considerations are the need to apply basic scientific principles (55, 304, 311). Using independent data to test the resultant models, complying with the limitations of chosen analytical or descriptive tools and data sets, and avoiding parameterization of models based on data sets with very narrow ranges of variation can achieve compliance. Often, apparently accurate statistical models fail to demonstrate predictive ability when tested against independent data rather than data derived by dividing a set of data and using one set for fitting and the other for testing the models (262, 278, 279). In addition, popular statistical models, like logistic regression and discriminant functions, rely on pattern matching with meteorological data and so cannot cope with novel climates or with extrapolation to other locations with different patterns of temperature and rainfall, even though they may describe the current range of a species quite accurately. Hence, such descriptive techniques are suited only to answering questions that involve small incremental changes in conditions within the existing ranges.
The ranges and relative abundance of two important African malaria vectors, Anopheles gambiae sensu stricto and A. arabiensis, have been related to temperature and a ratio of potential evaporation to rainfall as a measure of moisture availability (193). The population at risk from lymphatic filariasis in Africa was also related to these climatic variables (194). Using a combined model and rule-based approach, thresholds for temperature and rainfall have been inferred by using observations from areas of Africa with different malaria transmission patterns (68). The CLIMEX model (304, 311, 313) incorporates a hydrological model to describe the availability of moisture and so accounts for the effects of changes in temperature, rainfall, and evaporation when assessing risks from climate change. It automatically takes any temperature-moisture interactions into account when provided with appropriate meteorological data that include relative humidity or equivalent readings. CLIMEX has been used widely for risk assessments under climate change (303, 304, 307). The malaria transmission factors, biting and entomological inoculation rates, were predicted in Kenya using a soil moisture model (250). The model substantially improved the prediction of biting rates compared to rainfall, explaining up to 45% of A. gambiae biting variability and 32% of the variability of A. funestus when given different time lags.
Each species of vector has characteristic climatic requirements (194, 304) and vector competence for a given biotype of parasite (344) (29). This flags the need to keep each element of the disease triangle (Fig. 1) in mind because the climatic requirements of each vector-pathogen combination needs be taken into account in order to develop a realistic measure of risk (48, 304). Incorporation of species-specific vectorial capacity into global risk assessments has started (208). Integrated assessment frameworks are being developed to bring some of these elements together, with applications to malaria, dengue, and schistosomiasis (53, 205, 220, 248, 315). The use of spatial tools, such as geographical information systems and landscape ecology, in studies of vector management and global change effects on vector-borne diseases has been advocated (43, 97, 159).
Temperature is one such variable that varies systematically with latitude and altitude. The effect of altitude on temperatures is approximately equivalent to 5.7°C/km of elevation. The expected altitudinal range shift with increasing temperatures can be calculated using the formula (183)
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170 m in the elevation of a given transmission rate of vector-borne diseases. Warming over the past century has been 0.6°C (144). Thus, reported changes must be within the range of 100 m to have credibility. For example, one credible report is of an increase in height of the freezing point in the tropics of 110 m (83).
Similarly, expected latitudinal shifts in species ranges with global warming can be expected to be broadly consistent with effects of latitude on temperatures. The approximate formula (183)
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118 km. These figures provide a benchmark against which to relate reported changes in the distribution of vector-borne diseases with respect to global warming, but they need to be related to local modifying factors that create different microclimates and so change the actual area at risk. Similar benchmarks need to be provided for all other environmental and social variables, with rigorous interpretation of historical events that have often been poorly documented or misinterpreted.
Climate change has the potential to change the intensity of transmission of vector-borne diseases in addition to altering the exposure to the diseases by shifting the geographical distributions, as shown above. The extent to which the disease is sensitive to changes in transmission rates depends on a number of variables, including the responses of vector and pathogen to changes in the particular range of temperature or moisture concerned, and the immune status of the host population. Ideally, it would be useful to have a readily measurable benchmark against which to assess reported claims of involvement by climate in observed changes in the status of established vector-borne diseases. Unfortunately, the species-specific nature of the transmission dynamics of each pathogen renders that more difficult than the task of benchmarking changes in geographical distributions. However, it is still possible to match geographical locations with similar intensity of transmission by using models such as CLIMEX. Alternatively, mathematical models of the biological processes in the transmission cycle (also called mechanistic models) can be used to infer the sensitivity of the transmission rates of vector-borne diseases to changes in climate (189, 210, 212, 307). The major advantage of dynamic models over nonmathematical approaches or statistical models is that they are able to detect surprises or so-called emergent properties of systems that arise from discontinuities, such as thresholds or nonlinearities in biological processes.
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Climatic and nonclimatic global change drivers, such as human movements, land use and irrigation, and drug or pesticide resistance, can have large effects on disease transmission. Since some environmental changes are global but vary on a regional scale, the degree of exposure of each human-vector-pathogen system will vary with both the driver involved and the geographical location. The risks associated with each type of change need to be addressed on a disease-by-disease and location-by-location basis. An assessment of relative risks associated with each disease and global change driver is needed to prioritize the allocation of resources to adaptive measures. Such a rating system does not exist at present, and its production will require inputs from panels of experts. While most projected environmental changes appear to favor water-breeding vectors, temperature effects on other types of vectors are likely to be local and less severe.
While humans have different exposures to vector-borne diseases under each global change driver, the disease systems also vary in their sensitivity. The extent to which the incidence of a disease is sensitive to a nominated change at a particular geographical location depends on the interaction of the disease organism, its vector, its host population, and the environment (Fig. 1). The global change drivers are likely to have their greatest effect by influencing the numbers and seasonal patterns of activity of the vectors or by moving or accelerating the development of the pathogens. The degree of contact between hosts, vectors, and pathogens and the immune status of the host population will also be sensitive to change.
In most historical instances, the resurgence of diseases can be related to local ecological changes that favored increased vector densities or host-vector contacts, reintroductions of pathogens, or breakdown of vector control measures (121, 270). Development projects such as irrigation and water storage, urbanization, and deforestation have resulted in changes in communities of vectors, with increased population densities of certain species that led to the outbreaks of vector-borne diseases. Increased travel and transport have introduced infectious agents and vectors into new areas. The advent of global-scale environmental changes in recent decades has been an additional risk. The next sections review the evidence for the effect of environmental change on the key vector-borne diseases with likely future global change scenarios.
Extreme climatic events have major effects on the transmission rates of vector-borne diseases. In the light of expectations that climate change will increase the frequency of such events disproportionably, such extreme events may emerge as a more important feature of climate change than are changes in average climatic conditions. They are therefore considered in more detail below.
There have been a large number of studies and reviews of the sensitivity of vector-borne diseases to climate change (37, 40, 49, 50, 61, 62, 82, 84, 88-90, 110, 121, 123, 125, 126, 134, 164-166, 169, 186-189, 191, 192, 206, 209, 215, 220-223, 225, 228, 230, 245, 246, 249, 264, 266, 267, 269, 270, 295, 303, 307, 309, 310, 335, 350). The results have led to quite different perceptions of the role of climatic change and other factors in historical patterns of disease incidence.
The coherent pattern of the retreat of tropical glaciers, an upward shift in the freezing isotherm in the tropics, increases or decreases in the geographical ranges of temperate or Arctic species, respectively, at higher latitudes, earlier spring migration and breeding by birds, and earlier seasonal activity of insects have been cited as examples of impacts of gradual global warming (90, 125, 126, 243, 282). The observations were claimed to be consistent with increasing global temperatures and with model predictions. Taken together, these phenomena provide strong evidence that climatic changes in recent decades are already affecting up to 50% of the species examined in a survey of the literature (243, 282). There is no reason to believe that vector-borne diseases are exceptions to this experience of small and gradual changes in seasonal activity and expansion of ranges to higher altitudes and latitudes. The issue for workers in the field is to establish adequate baseline data on seasonal transmission patterns, prevalence of disease and geographical distributions, benchmarks to monitor and assess the consistency of changes with known physiological processes, and sufficiently accurate monitoring data in strategic locations to be able to detect the changes as they occur around species range boundaries initially. Only then will the medical community be able to separate the subtle effects of climate change on vector-borne diseases from the more obvious effects of other factors.
A number of authors have raised the possibility that global warming may have played some part in the recent range expansions and outbreaks of vector-borne diseases (37, 40, 89, 90, 125, 163, 186, 188, 197). Two types of climatic effects could theoretically have been involved. First, changes like the ones observed for other species of plants and animals referred to above will gradually increase the transmission rates in cooler climates and so extend transmission into previously disease-free areas while slowing transmission in areas that become too hot. In some cases, realization of this expectation with vector-borne diseases will be different for other species because often the vectors are already there but the pathogens have been eliminated. Second, changes in the intensity of extreme climatic events will alter the patterns of epidemics. Any change in the intensity and frequency of extreme climatic events may take decades to detect against a background of insufficiently long historical records and high climatic variability with ENSO-like events, and it is probably too early to invoke this effect in any historical events.
Other authors (34, 121, 136, 266, 270, 294), citing historical outbreaks and identifying the largest current signals in a set of data, concluded that other factors were more important than climate and questioned the veracity of claims (90, 197, 206, 223) that anthropogenic climate change could have contributed to the epidemics. For example, it has been suggested (34) that replacement of forest by agriculture provided new habitats for breeding of mosquitoes at Usambara in Tanzania, rather than local temperatures rising as a result of land clearing, as was previously suggested (214). The role of climate change in an outbreak of malaria in Rwanda (197) was questioned because it coincided with a change in detection methods that was more likely to explain the jump in reported incidence of infections (270). Opposing interpretations of historical temperature data in East Africa, based on interpolated meteorological data (235), led to different interpretations of the role of global warming in the observed increase in incidence of malaria in recent decades (136, 247; J. A. Patz, M. Hulme, C. Rosenzweig, T. D. Mitchell, R. A. Goldberg, A. K. Githeko, S. Lele, A. J. McMichael, and D. Le Sueur, Letter, Nature 420:627-628, 2002). A negligible role was seen for global warming in the resurgence of vector-borne disease in Latin America, Africa, and Asia in the past two decades (121, 266, 270, 294). It was claimed to be inappropriate to use climate-based models to predict future prevalence because climate plays a small role in disease outbreaks (270). That view does not take sufficient account of the role of climate in determining the underlying seasonal phenology or geographical distributions of vectors and pathogens. Neither does it recognize the contribution of climate-based modeling in allowing researchers to extrapolate results from one geographical location to another. What has been missing from the global change studies is adequate inclusion of nonclimatic variables in the analyses, which reflects the difficulty in building and maintaining global databases of local environmental changes.
In a more pragmatic view, global warming was considered to be unlikely to cause major epidemics of tropical mosquito-borne disease in the United States (121) and Australia (48) as long as the public health infrastructure and living conditions remain the same. It is not surprising that the role of climate change in historical events has been contentious because the extent of the changes is only just beginning to be large enough to be distinguished from natural variability and the events were not sufficiently well documented to ensure that all variables could be accounted for. Despite the differences in emphasis and focus on historical or future events, all authors agree that there are multifactorial causes of change in the incidence of vector-borne diseases. Land use events will be more important in the short term, but climate change has the potential to be important in the longer term.
Climate change will affect both the invertebrate vectors and the development of pathogens in those vectors. Basic biological considerations indicate that with global warming, the duration of the growth season will increase, allowing more generations of vectors each year in cooler areas. Development is prevented at low temperatures, but as temperatures rise, a race develops between parasite development and accelerated mortality of the vector. The winters will be shorter and less severe and so will reduce the mortality rates of species of vectors that are currently limited by low temperatures. Other temperate species of vectors are insensitive to winter conditions in some environments (270). In some environments, temperatures will rise to levels where the mortality rates of the vectors are so high that they die before being able to transmit a pathogen. Changes in future moisture regimens are much more uncertain.
Malaria (i) Exposure and sensitivity Most of the analyses of the impacts of climate change on vector-borne diseases have been aimed at malaria, consistent with the dominant global impact of that disease. The initial emphasis has been focused on the direct effects of changes in temperature on development of the parasites and longevity of the adult mosquitoes. This reflects the ease of investigating temperature effects rather than their relative importance compared with other drivers of change. Small increases at low temperatures were shown to increase the risk of transmission disproportionately, and it was concluded that vulnerable communities in malaria-free areas or those with unstable malaria are likely to be at increased risk of future outbreaks (189). An increase of 12 to 27% in the epidemic potential of malaria transmission compared with current areas of endemicity has been projected as an indication of the sensitivity of malaria to climate change (209).
Modeling studies indicate that higher temperatures will lead to an increase in the population that is exposed to malaria as a result of an expansion of the geographical distributions of vector-borne diseases into higher altitudes and latitudes (49, 50, 189, 192, 211-213, 248). A mathematical model, designed to identify malaria epidemic-prone regions, was used to explore possible changes in epidemiology with projected global climate change in the African highlands (192). It was assumed that free water for breeding sites would be available when higher temperatures occur because water is not currently limiting. Most malaria epidemics in the endemically unstable highlands are due to Plasmodium falciparum, the cause of the most severe form of clinical malaria. A plea was made to accord these areas special status and recognize them as having a high risk under climate change.
Europe has experienced significant warming in recent decades, and there is evidence of climatic effects in the northern spread of tick vectors in Sweden (165). Nevertheless, the current geographical range of malaria in Europe is much smaller than its potential range as shown from historical records (148, 149, 191, 269, 303). In many regions the vectors are present but malaria transmission does not occur because the pathogens have been eliminated. An increase in average temperature has the largest effect on epidemic potential where parasite development is limited by low temperatures in temperate areas, consistent with the conceptual models in Fig. 8 and 9. Infected mosquitoes introduced through airports are also likely to survive longer in the future if there is increased rainfall and will therefore enhance the problem known as airport malaria (295).
A claim that Australia was highly vulnerable to malaria under climate change (233) has been refuted (48, 332). The suitable area is determined mostly by the climatic requirements of the only highly competent vector, A. farauti, rather than the temperatures required for the development of malaria parasites (48, 304). The CLIMEX model was used to determine the area at risk of malaria after an increase in temperature, so any reduction in soil moisture due to increased evaporation at the higher temperatures was factored into the calculation. An increase of 1.5°C was expected to allow A. farauti to colonize Gladstone, a town on the east coast of Australia 800 km further south of its current range limit, with islands even further south being potential habitats. The results exceed the benchmark for the effects of such a temperature rise and illustrate the need to consider localized effects of topography on likely range expansions. Whether this potential is realized will depend on many other variables, particularly the state of the public health system. More recently, the mosquito has been detected at Mackay, 2° south of the previous southernmost record near Townsville (328). The finding confirmed earlier unpublished records and is not thought to relate to any change in temperatures.
Both the direct and indirect effects of increased temperature on anopheline mosquitoes, malaria parasites, and their hosts have been examined (295). It was concluded that the most likely effects of climate change would be on the availability of surface water for larval habitats. It may also be assumed that any increase in the density of foliage of plants growing in an enriched CO2 atmosphere will provide more favorable shelter for adults of some species of mosquitoes, extending their longevity. If the residual soil moisture also increases as the water use efficiency of plants increases, there may also be an increase in the amount of surface water during the season and the expanded range of sheltered habitats referred to above. These scenarios are still highly speculative.
A descriptive, statistical model was used to challenge claims that the global distribution of P. falciparum malaria is likely to increase significantly under climate change (280). Several comments about this analysis are necessary. First, it was claimed that little change is likely in the area at risk because those areas, which become more receptive with higher temperatures, will suffer increased moisture deficits. This point had been noted previously (148), but as we saw above, moisture-related climate change scenarios are still too uncertain to be useful. The complicated relationship between the incidence of malaria and floods and droughts makes the task even more difficult. Second, the current distribution of "malaria," used to define the current global area at risk, was not very specific and the analysis did not take into account the diff
