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Aircraft and ships are believed to be directly responsible for rapid expansion in the range of many plants and animals via inadvertent transport Perrings et al. Here we briefly review some of the major invasion events facilitated by transport, and demonstrate some approaches to the prediction of future disease vector invasions.
Though the mosquito is now established throughout the tropical and sub-tropical regions of the world, it was located solely in West Africa until the 15th century Lounibos, At some point, the insect adapted to anthropogenic breeding sites, such as water storage jars in ships Lounibos, This ability enabled it to take full advantage of the growing slave trade from West Africa to reach the new world or to invade Portugal and Spain before its proliferation elsewhere on European ships.
Intensive control and eradication schemes in the s and s reduced its extent Gubler, a. Gradual resurgence following the end of these control campaigns has resulted in the species once again becoming wide-spread across the Americas, and associated with the emergence of dengue and dengue haemorrhagic fever Gubler and Clark, Perhaps the most devastating introduction of a disease vector of recent times was that of An. Its gradual spread over 10 years into 54 km 2 of Northeast Brazil led to extensive malaria epidemics, costing 16 lives and around 3 billion USD modern day estimate in healthcare, drugs and the vector eradication programme Killeen et al.
These epidemics were based solely on the greater vectorial capacity of An. Similarly, high mortality rates were seen on Mauritius when An. Control efforts ended the epidemics, but low-level and localized rural transmission continues. Native to Japan, Southern China and Korea where the larvae develop in natural and artificial containers, its likely mode of introduction was through tyre shipments. Since the initial introduction, the mosquito has spread to Connecticut Mustermann and Andreadis, , Maryland, Pennsylvania and Ohio Lounibos, The discovery of wild-caught Ae.
The Asian tiger mosquito, Ae. The range expansion of Ae. The mosquito spread from its range initially to the Pacific Islands Gratz, in the s and then, within the last 20 years, to other countries in both the Old and New Worlds Moore and Mitchell, ; Gratz, This is thought to have been through ship-borne transportation of eggs and larvae in tyres Reiter and Sprenger, ; Reiter, The spread of Ae. Figure 2 shows its extent in The Old World distribution of Ae. Counties of the United States of America reporting the presence of Ae. Developing approaches to highlight routes of the greatest risk of invasion by disease vectors within the global transport network is an important prerequisite to planning effective control and disinsection efforts.
Although distance may no longer represent a significant barrier to vector traffic, climate at the point of entry still presents a fundamental constraint to establishment, since poikilothermic arthropods are very sensitive to the weather. Here we review an approach, first outlined in Tatem et al.
Major international seaport names, locations and estimated number of ships per annum between each were obtained from Drake and Lodge The data consisted of the estimated number of ship visits in to the most frequently visited ports. Data on a total of routes between international airports in the year were therefore available. Gridded meteorological data New et al.
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The mean, maximum and minimum temperature, rainfall and humidity measurements were extracted to produce nine climatology surfaces. Dendrograms are visual representations of the results of hierarchical clustering described below that are commonly used in the fields of evolution and genetics, and occasionally in an environmental context Sugihara et al. Here, dendrograms are used to provide a climatic representation of the global air and sea transportation networks, a method first outlined in Tatem et al.
This requirement was not met for airports located coastally or on small islands or for the majority of seaports. In these cases, reduced numbers of land pixels were extracted. These signatures represented a quantitative description of the climatic regime at each seaport and airport, in terms of temperature, rainfall and humidity. Euclidean distance is defined as the shortest straight-line distance between two points: A simple test using other distance measures e.
The climate dissimilarity matrices were subject to hierarchical clustering using an agglomerative algorithm Webb, Hierarchical clustering procedures are the most commonly used method of summarising data structure Webb, The clustering process produces a hierarchical tree, which is a nested set of partitions represented by a tree diagram, or dendrogram.
The clustering results here were translated into dendrograms based on centroid linkage. Figures 3a and b show the climatic dendrograms for the major seaports and airports, respectively. In both figures the inset close-up shows the branches of significance to the dispersal of Ae. The seaport and airport locations were overlaid on the historical Ae.
This allowed for the fact that Ae. Ninety percent of airports within the pre-expansion distribution of Ae. Each matrix was rescaled independently to a range of 0—1 and the results for the climatic matrix then inverted so that values near to 1 represented similar climates and values close to 0 represented dissimilar ones.
Values in the two rescaled matrices for any pair of ports—one with and one without the invading species in question—were then multiplied together to estimate the relative risk of invasion and establishment. When these are multiplied, we arrive at a disease vector invasion risk of 0. Table 1 details the top 20 shipping routes from over 20 possible routes and Table 2 shows the air travel routes from over possible routes identified as having the highest relative risk of Ae.
There is correspondence between the predicted risk routes in Table 1 and the global invasions or interception of Ae. Three of the top 10 shipping routes run from Japan to the south-east United States, where some of the earliest breeding populations of Ae. Genoa, the destination of five more routes from Japan in the top 20, was one of the earliest European cities to report Ae.
Of the remaining routes in Table 1 , interceptions of Ae. No documented evidence exists of invasion by Ae. The relative importance of sea traffic volume and local climate in the establishment of Ae. Twenty-one ports are within the original range of Ae. Within this group of 47 ports, the average climatic distances of the 24 invaded and 23 non-invaded ports were identical, but sea traffic volumes were 2.
Sea traffic volumes, therefore, appear to make an important contribution to relative invasion risk. Although air travel was not implicated in the spread of Ae. The large air traffic volume running from Tokyo to Hawaii identifies this route as providing over double the risk of invasion as the others in Table 2. Details on Hawaiian ports were not available in the sea traffic database.
In every one of the top 20 high-risk air routes, Ae. In addition to determining at which seaport or airport an accidentally introduced disease vector is likely to become established, it is important to identify the areas to which vectors may subsequently spread. This was tested for Ae.
Given that the origin of the invasive Ae. Comparison with maps of known Ae. The dark regions indicating climatic similarity to Chiba across Europe and in South Africa, Australia and New Zealand, indicate that given the opportunity provided by transport networks, Ae. Future work on invasion risk should focus on the incorporation of data on land transport routes, human population distribution and how these relate spatially to endemic disease regions.
Darker shades represent areas with climates more similar to that of Chiba. This section reviews briefly the movement and emergence of vector-borne diseases through global human transport, and outlines approaches for highlighting areas at risk from future events. Outlined in detail in Rogers et al. The enforcement by the World Health Organization of yellow fever vaccination requirements for travel to endemic regions, and consequent minimal movement of the disease, demonstrates the effectiveness of global control measures.
Despite advances in preventative measures and the existence of a reliable vaccine, yellow fever outbreaks and epidemics have increased in recent years, particularly in Africa Mutebi and Barrett, Many of these epidemics have been caused by the large-scale movements of susceptible individuals into high yellow fever risk zones and by the neglect of control procedures Mutebi and Barrett, The past 30 years has seen a marked global emergence and reemergence of epidemic dengue, with more frequent and larger epidemics associated with more severe disease Mackenzie et al.
Fuelled by the expansion of the range of its principal vector, Ae. The global air transport network is not only aiding the spread of both dengue vectors and virus serotypes within tropical regions suitable for transmission, but also facilitating a substantial increase of imported cases elsewhere Jelinek, ; Frank et al. It circulates mainly among birds, but can infect many species of mammals, amphibians and reptiles Dauphin et al.
The appearance of WNV in New York in and its subsequent spread westwards across the United States Petersen and Hayes, and into Central America represents the best-documented movement of a disease in recent times Granwehr et al. Spread by many different species of mosquitoes and the movement of birds, it is less influenced by human transportation networks than other diseases discussed in this review, but its arrival in the US in is thought to be associated with some form of commerce or human travel.
With changing climate, coupled with increased human movement and spread of exotic mosquitoes via global transport networks, the risks of further WNV outbreaks are a distinct possibility Granwehr et al. General socio-economic improvement, combined with wetland drainage and other water resource development, improved housing, better animal husbandry and wider availability of quinine resulted in the decline of indigenous malaria in high-income countries during the 19th and 20th centuries Hay et al.
In contrast, increasing tourism and human migration has meant that malaria continues to be imported into high-income countries, which have been classified as free of malaria transmission. Numbers vary, but it is estimated that as many as 40 cases of malaria a year occur in Europe alone Toovey and Jamieson, This influx of infected travellers poses two major hazards: The last 25 years have seen both the numbers and types of malaria imported to high-income countries change significantly.
Figure 5a shows that the UK consistently had — cases of malaria every year reported since However the proportion of P.
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Figure 5b demonstrates that while the USA has fewer imported malaria cases annually than the UK, the trend towards increasing numbers of P. The rise in P. The precise causes of the decline in imported Plasmodium vivax cases and increase in those of P. The increasing level of malaria movement also has the effect of enhancing the possibility and speed of drug-resistant malaria spread.
Since the first reports of chloroquine resistance 50 years ago, drug-resistant malaria has posed a major and increasing problem in malaria control Hastings and Mackinnon, ; Anderson and Roper, ; Hastings and Watkins, Chloroquine resistance is now worldwide, while resistance to newer drugs is appearing in many regions, especially in South-east Asia, where multidrug resistance is a major public health problem Wongsrichanalai et al.
The growth in global travel and human migration is assumed to have caused this spread, with the speed of spread of resistance mirroring its expansion. Though chloroquine remained effective for some 20 years before signs of resistance emerged, it is unlikely that a similar period of grace can be realistically expected for recently deployed treatments given the current levels of global travel Hartl, Between and , 87 suspected cases were recorded, with almost all being P. Figure 6 summarises the locations and time of year of these probable airport malaria cases. For example, in a three-week period in , it was estimated that — Anopheline mosquitoes were imported into France by — aircraft arriving from malaria-endemic regions of Africa, at the rate of 8—20 Anopheline mosquitoes per flight Gratz et al.
The ever expanding global transport network, increased travel to malaria-endemic countries and a decline in aircraft disinsection Gratz et al. Data taken from Alos et al. The establishment of a vector-borne disease in a new area from an endemic region can be caused either by movement of an infected host and availability of competent vectors in the new area, or the invasion, if only temporarily, of an infected vector.
Here, we extend the methodology outlined in Section 3. While globally, the movement of P. Additionally, the possible effects of invasion of malaria endemic regions by An. The likelihood, however, of a more than very temporary establishment of P. Unsuitable year-round climate, An. Malaria caused by P. Although malaria has been eradicated in the UK, re-introduction is theoretically possible Hay et al. This risk is negligible, however, as the majority of the former habitats of An.
This is supported by the analyses presented above and the fact that not one of the 52 imported malaria cases reported since has led to a secondary case. The growth of travel to Africa therefore presents a negligible risk of the establishment of malaria in the UK. The approach described here follows on from that described in Section 3. Monthly gridded climatologies were acquired New et al.
Climate dissimilarity matrices were created for each month, and these were clustered hierarchically to create 12 global airport dendrograms, one for each month of the year. Airport malaria cases represent instances where imported infected mosquitoes have caused autochthonous malaria transmission and, therefore, were used to define climatic suitability thresholds on each dendrogram.
Malaria seasonality maps for Africa Tanser et al. Finally, the situation in was examined using the air traffic database described in Section 3. Table 3 shows the 18 routes identified as at risk for P. Comparison with Figure 6 shows excellent correspondence with the timing and location of actual suspected cases of infected-mosquito importation and autochthonous transmission.
Year air travel risk routes for possible temporary P.
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The results indicate that many airports in other regions of the world are more favourable climatically for Anopheles survival, and for many more months of the year than European destinations. The concentration of major airports in the temperate north means that July summer in this region on Figure 7 shows the largest number of potentially suitable destinations climatically, mainly linked to West African airports, including those in Europe where most SSA air traffic is directed, causing cases of airport malaria in the summer months particularly in unusually hot and humid periods.
The other three months on Figure 7 show considerably fewer at risk airports, though throughout the year, Caribbean and Central American airports are highlighted consistently, indicating that their climates vary in synchrony most closely with the cycle of African malaria transmission seasons. Non-SSA airports that are similar enough climatically to the SSA airports within their primary malaria transmission season for possible P. The current heavy bias of SSA air traffic to European destinations has resulted in around two cases a year of airport malaria in the summer months, when particularly hot and humid conditions can be suitable for temporary Anopheles survival, and occur in synchrony with West African transmission seasons.
The effects of opening up new air routes from malaria-endemic African countries to non-European destinations, where conditions are more suitable for Anopheles survival and are synchronous with African malaria transmission seasons year-round, could therefore have serious and largely unexpected consequences.
Increases in global travel are occuring simultaneously with many other processes that favour the emergence of disease Wilson, Travel is a potent force in disease emergence and spread, whether it is aircraft moving human-incubated pathogens, or insect vectors, great distances in short times, or ships transporting used tyres containing mosquito eggs.
With no apparent end in sight to the continued growth in global air travel and shipborne trade, we must expect the continued appearance of communicable disease pandemics, disease vector invasions and vector-borne disease movement. Approaches that can model, predict and explain such events can be used to focus surveillance and control efforts efficiently.
This review has shown that the risk of movement of infectious diseases and their vectors through the global transportation network can be predicted to provide such information. Future challenges must focus on incorporating information on temporal variations in passenger numbers, stopover risks, intra-species competition, human populations at risk, breeding site availability, possible climate change, disinsection and land transport, as well as quantifying the relative importance of all types of transport for vector and disease movement.
We are especially grateful to John Drake for the generous supply of sea traffic data. National Center for Biotechnology Information , U. Author manuscript; available in PMC Jul Tatem , 1 D. Rogers , 1 and S. Author information Copyright and License information Disclaimer. The publisher's final edited version of this article is available at Adv Parasitol. See other articles in PMC that cite the published article. Abstract Air, sea and land transport networks continue to expand in reach, speed of travel and volume of passengers and goods carried.
Plague More than million people are thought to have been killed by bubonic plague in three major pandemics between the 14th and 17th centuries Duplaix, ; Eckert, Cholera Cholera is caused by an intestinal infection with the bacterium, Vibrio cholerae , leading to severe dehydration, shock and often-rapid death Sack et al. Influenza The influenza virus is remarkable for the rapidity with which it can spread, the brevity of immunity it confers and its genetic variability McNeill, ; Ferguson et al. Severe Acute Respiratory Syndrome Severe acute respiratory syndrome SARS is a coronavirus that adapted from animal hosts to become readily transmissible between humans Peiris et al.
Bioterrorism While bioterrorism has been at the forefront of public health planning since the 11 September attacks on New York, it has a long history. Predicting, Modelling and Controlling Future Pandemics Numerous approaches have been developed which attempt to capture the possible future movements of newly emergent communicable diseases through global and local transport networks Thomas, ; Haggett, Airlines and Aircraft Manufacturers 7.
Commercialism and the Culture of Production Pt. Liberalization and Privatization, 8. The United Kingdom more The United Kingdom 9. Online Table of contents Broken link?
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