Global Health Impacts of Vector-Borne Diseases Workshop Summary (2016) / Chapter Skim
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Workshop Overview
Workshop Overview
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Over the past three decades, previously controlled vector-borne diseases have resurged or reemerged in new geographic locations, and several newly identified pathogens and vectors have triggered disease outbreaks in plants and animals, including humans. A variety of factors underlie this trend among emerging vector-borne diseases, including • The rapid expansion of global travel and trade, enabling the geographic spread of pathogens, vectors, and animals that serve as so-called reser voirs2 of disease; 1 The planning committee's role was limited to planning the workshop, and the workshop sum mary has been prepared by the workshop rapporteur as a factual summary of what occurred at the workshop.
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Furthermore, the ranks of scientists trained to conduct research in key fields including medical entomology, vector ecology, and tropical medicine have dwindled, threatening prospects for addressing vector-borne diseases now and in the future. In June 2007, as these circumstances became alarmingly apparent, the Forum on Microbial Threats hosted a workshop to explore the dynamic relationships among host, pathogen(s)
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From the perspective of infectious diseases, vectors -- which can be either living (biological) or nonliving (mechanical)
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• Plasmodium knowlesi -- This very rare species is found in parts of South East Asia. Source: http://www.nhs.uk/Conditions/Malaria/Pages/Causes.aspx (accessed March 25, 2016)
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. Infectious disease outbreaks resulting from such spillover events include epidemics of West Nile viral fever in the United States and of Rift Valley fever in Africa and the Middle East.
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. Figure WO-2 illustrates major taxonomic pathogen groups causing emerging infectious disease in plants.
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introduction of pathogens causes the most plant emerging infectious diseases; (c, d, and e) factors cited as the cause of disease emergence for bacteria (c)
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. Epidemics have also arisen in naïve host populations, whose exposure to vector-borne diseases has increased with the globalization of travel and trade, and with the decline of vector control efforts.
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. She described several emerging ector-borne v plant diseases that threaten U.S.
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. Vector-Borne Diseases of Concern in the United States Humans are incidental hosts for most mosquito-borne viruses including WNV, as well as for tick-borne pathogens, which include Borrelia burgdorferi (the bacterial cause of Lyme disease)
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Many of these cases occurred during three major outbreaks, which took place in 2002, 2003, and 2012 -- all during heat waves, he added. As illustrated in Figure WO-5, certain geographic regions of the United States seem to be at higher ecological risk for West Nile viral disease compared to other regions of the United States.
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Dengue virus now infects about 400 million people each year, having resurged after DDT-based vector control efforts were halted in the 1970s, according to Petersen. Dengue's expansion has also been abetted by the introduction of an additional vector species, Aedes albopictus, from Asia to the United States in 1985 (in a shipment of used tires)
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Today, in tropical locations such as Puerto Rico, over 90 percent of residents have already been infected by DENV, Petersen stated. Can dengue fever -- once a common illness in the southern United States -- reemerge in this country?
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Data from Pan American Health Organization. find these huge outbreaks on the Mexican side of the border, just right across the Rio Grande River." His group's investigation of this paradox revealed vastly different human behaviors and environments in adjacent towns on either side of the border, and suggested that the lack of air conditioning and more crowded living conditions in Matamoros, Mexico, resulted in much higher rates of dengue transmission in comparison to Brownsville, Texas (Ramos et al., 2008)
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Data from Pan American Health Organization.
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More broadly, he observed, ecological parameters of pathogen transmission remain largely unknown, which limits the usefulness of disease models -- as does the fact that many communities are not prepared to respond to vector-borne disease threats owing to inadequate surveillance and/or mosquito control capacity. For prevention and treatment, "The glass is only half full," Petersen noted.
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Around the time that the glassy-winged sharpshooter invaded California, plant pathologists relied on studies of pathogen host range, epidemiological surveys, and the outcomes of vector control measures attempted in the field to inform mitigation efforts. These ecologically based methods were sufficient to manage diseases within a limited geographic area and time frame -- a sensible approach, prior to the global transmission of economically important diseases, he said.
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"It is really an interesting problem that goes way beyond a plant disease and how to manage it." How do plant diseases actually move to new ecosystems? In many cases it occurs on ships, according to Almeida, as contrasted to their human counterparts, which move readily by air travel.
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In some cases where that is true, he suggested, controlling vector populations and their ability to spread pathogens to humans or animals offers relatively simple routes to reducing disease transmission, as compared with pathogens that follow multiple transmission routes between animals and people, and are therefore more prone to spillover. The identification of land use change and international travel and trade as primary drivers of emergence of vector-borne animal diseases should guide disease surveillance and prevention efforts, he added.
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If they are negative it means they are free of the disease." On the other hand, he continued, the disease can be disastrous for individual farmers, who operate on small economic margins. Vector control might seem a reasonable way to reduce disease transmission, but it would not be an easy route to take, given our limited understanding of the ecology of the widespread midge, he observed.
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Therefore, it may be equally important to develop a targeted, effective approach to disease control that will enlist the support of people and governments. A better strategy against Rift Valley fever in South Africa might take advantage of herd immunity, which also appears to influence outbreak patterns there, he observed.
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Limited resources were available to respond to another peak outbreak in 2012. While it is now possible to make accurate local predictions of WNV outbreaks in time to prevent their occurrence, Petersen said, communities are not investing in local surveillance, nor are they willing to implement vector control measures in advance of human cases of the disease.
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Vector-borne plant diseases pose an especially difficult problem for surveillance, according to several participants. Until a plant disease becomes epidemic, it is perceived as a problem only to the farmers whose crops are infected, Almeida noted.
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24 GLOBAL HEALTH IMPACTS OF VECTOR-BORNE DISEASE and economical consequences. "I think there will be a push for incorporating social sciences into what we do," Almeida predicted, and offered as an example the work of a postdoctoral researcher in his laboratory (Dr.
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-- offers hope that these trends may be reversed. Forum member Kevin Russell of the Armed Forces Health Surveillance Center pointed out that the Global Health Security Agenda emphasized a multisectorial approach to global health security, which depends in part upon the economic ramifications of plant, animal, and human diseases.
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This point was illustrated again and again over the course of the workshop, through the lens of various vector-borne diseases in natural, agricultural, urban, and suburban contexts. CHANGING DISEASE PATTERNS Four speakers illustrated the dynamic nature of vector-borne diseases in presentations describing the evolution and epidemiology of dengue and chikungunya, shifting patterns of insect-borne parasitic infections closely associated with poverty, leishmaniasis and Chagas disease, and the recent range expansion of multiple tick-borne diseases in the United States.
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Experiments in mosquitoes showed that both genotypes were equally capable of binding the insect's midgut, but that the Southeast Asian virus was more prevalent in the salivary glands, and therefore more available for transmission to humans, she added. Both features contribute to the 60-fold-higher transmission efficiency of the Southeast Asian genotype, which in turn explains its ability to displace the American genotype, she concluded.
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Recent evidence shows that the Asian genotype can be transmitted with equal efficiency by both mosquito vectors, one of which -- Aedes albopictus -- is well adapted to temperate climates (Vega-Rua et al., 2014)
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The symptoms of dengue fever can resolve within a week, or during the same period it can progress to severe hemorrhagic disease or death, Margolis noted. Many of dengue's symptoms resemble those of several other febrile diseases, such as leptospirosis.
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Dynamics of Leishmaniasis and Chagas Disease Two vector-borne parasitic diseases, leishmaniasis and Chagas disease, are strongly associated with poor living conditions that expose people to the insect vectors that carry them. "These are diseases of poverty," observed speaker James Maguire, of the Harvard Medical School.
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This is a parasite that is definitely on the move." Maguire presented the following examples to illustrate the spectrum of drivers that influence leishmaniasis' transmission patterns and geographic range: • Cutaneous leishmaniasis, present in the Americas prior to human arrival, has recently exhibited increased incidence and broadening geographic range in response to human incursions into the forest (e.g., chicle harvest ing) and the expansion of human settlement to formerly forested areas.
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The introduced vector spread through Central America along the Pan American highway and beyond, becoming more important in this new territory than the native vector for Chagas disease. Maguire recalled that when poor migrants from rural
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A number of obstacles stand in the way of eliminating Chagas disease altogether in these regions, Maguire noted: • the re-infestation of houses with sylvatic T infestans or other sylvatic triatomine bugs that can adapt to domestic environments; • passive transport of alternative vectors from other regions; • the development of insecticide resistance by vector species; and • ongoing migration from rural to urban areas.
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paradigm changes in terms of vector and ecology associations with these pathogens." In particular, he noted, human activity has profoundly affected tick-borne infections, which continue to shift in scope and magnitude. As an example of this trend, Paddock described recent changes in the epidemiology of Rocky Mountain spotted fever (RMSF)
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Deer are keystone hosts for the two most important vector species of tick-borne pathogens in the United States, namely black-legged ticks (Ixodes scapularis) , known to transmit at least seven different human diseases, including Lyme, and Lone Star ticks (Amblyomma americanum)
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aegypti (see section on "History and Current Challenges of Dengue Vector Control" for a detailed account of this effort and its aftermath)
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. Based on a foresight study conducted by ECDC in 2008, Europe is at risk of vector-borne disease threats owing to anticipated changes in drivers of infectious diseases by 2020.
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Given the disproportionate contribution of global and environmental change drivers to vector-borne disease threats in Europe, the ECDC turned to infectious disease experts for advice in crafting strategies to meet these challenges. Many of these experts considered climate change to be of particular concern as a driver of selected vector-borne disease such as Lyme disease, West Nile viral fever, tickborne encephalitis, and leishmaniasis, Semenza stated (Semenza et al., 2012)
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FIGURE WO-10 EID drivers and plausible scenarios. NOTE: R&D = research and development.
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In addition to these applications of the E3 Network, the ECDC has compiled a handbook with practical climate change adaptation measures for infectious diseases: Climate Change and Communicable Diseases in the EU Member States15 (Ebi et al., 2013)
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A 2005 Council of State and Territorial Epidemiologists (CSTE) survey of state and selected local health departments found that federal funding had enabled the development of broadbased, multisectorial WNV surveillance capacity in all states and recommended that states be permitted to expand the use of ELC funding to more broadly address vector-borne disease surveillance (CDC, 2006)
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Due in part to decreases in ELC funding, he observed, "The ability to rapidly detect emerging and outbreak level threats and thus initiate prevention activities has clearly been compromised." The CSTE report recommends that the CDC examine national arboviral surveillance capacity and secure additional support as needed to ensure mosquito surveillance occurs in all metropolitan areas with historically high West Nile viral disease burden (Hadler et al., 2014)
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3. They have a surveillance system that includes mosquito surveillance to routinely monitor both larval and adult arboviral activity in all parts of the jurisdiction in which there is the potential for human outbreaks of arboviral disease based on past experience.
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Although most WNV infections are asymptomatic, interventions introduced less than 1 year after the first transfusion-associated cases were identified greatly 16 The August 2009 issue of Transfusion included a supplement on emerging infectious disease (Stramer et al.) agents and their potential threat to transfusion safety.
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Investigational testing under way in Puerto Rico since 2010, however, has produced comparable results to established WNV protocols, she reported. In retrospective tests of more than 15,000 blood donations acquired at the peak of the Puerto Rican dengue epidemic, about 1 in 500 samples tested positive for DENV (Stramer et al., 2012)
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. Concerns about the blood supply in Puerto Rico, which has become endemic for CHIKV, and in the United States at large, have been discussed and are summarized below (Katz, 2014)
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, so the three can occur quite successfully together." Because of these risks, several research blood donation screening interventions and pathogen reduction have been introduced in remote settings where importing blood components is not feasible, she explained. Low Threat for Chagas Few cases of blood-borne Chagas disease have occurred in the United States, Stramer reported, and blood-borne transmissions have only been documented by platelets, due to the fragility of the parasite (platelets are stored at room temperature and agitated to promote oxygen availability, likely enhancing survival of the parasite over their 5-day shelf life)
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. He described how he and coworkers investigated a series of extreme weather events between 2010 and 2012 that strongly affected agricultural production in major growing regions of Australia, East Africa, Russia, Southern Africa, and the continental United States -- and where, sometimes simultaneously, outbreaks of vector-borne diseases (including dengue, Rift Valley fever, and West Nile virus disease)
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Global patterns of floods and droughts influence the emergence, propagation, and survival of mosquito vectors and ultimately the transmission of mosquitoborne pathogens associated with diseases that include Rift Valley fever, dengue and dengue hemorrhagic fever (DHF) , and chikungunya, he explained (Anyamba et al., 2012; see adaptation, Linthicum et al., in Appendix A7)
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While extremes of temperature and precipitation have significant implications for the emergence and spread of vector-borne diseases, the magnitude of ENSO influence on some of these extremes cannot currently be predicted, Linthicum cautioned. Disease transmission dynamics in different environments and populations may vary widely, he observed, reflecting a broad spectrum of influences on vector species, vector population sizes, and vectorial capacity.
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SOURCES: NOAA, 2015; Reynolds et al., 2002. Globalization, Land Use, Global Warming, and the Invasion of West Nile Virus Continuing the discussion on WNV, A
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52 FIGURE WO-14 Potential El Niño regional teleconnections with patterns of vector-borne disease, rodent-borne disease, water-borne disease, and environment-linked respiratory illness patterns. NOTE: CHIK = chikungunya; CHOL = cholera; DENG = dengue fever; HFRS = hemorrhagic fever with renal syndrome; HPS = hantavirus pulmonary syndrome; MAL = malaria; PL = plague; RI = respiratory illness; RVF = Rift Valley fever.
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WORKSHOP OVERVIEW 53 FIGURE WO-15 Anthropogenic processes that facilitate the introduction and establishment of novel pathogens and increase their transmission. Trade, travel, and animal movement introduce new pathogens.
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involved in any given place in West Nile Virus transmission, and even relatively few bird [species] involved as well, and I think that's actually quite good news." Kilpatrick quickly noted that he and coworkers found that WNV has evolved since its introduction to be transmitted more efficiently by mosquitoes (Kilpatrick et al., 2008)
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Far more immediate than the anticipated effects of climate change, daily temperature ranges and extremes in temperature influence pathogen transmission, he stated, and these effects are tempered by other environmental factors -- claims he illustrated with examples from his work on malaria. Diurnal Temperature Range Malaria, Thomas observed, is the most important and longest studied of all vector-borne diseases, yet there remain "massive gaps in our knowledge." Taking what he termed a mechanistic approach, he began his remarks by explaining the components of vectorial capacity, a measure of the transmission potential of a vector population (a specific mosquito species, in the case of malaria)
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. The results, shown in Figure WO-16, reveal that while diurnal temperature variation did not have a significant effect on survivorship under optimum mean temperature conditions, similar variation under high average temperature conditions slows development, he reported -- and "the bigger the daily temperature variation the worse things get," he said.
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At the standard temperature for raising mosquito vectors of malaria, 27°C, about half of the mosquitoes of both species became infected, he reported; if the mean temperature increases, fewer mosquitoes become infected. Diurnal temperature range exaggerates this effect, and at high temperatures and broad range, inhibits infection altogether, they found.
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Moreover, he later noted, "If we're going to understand local transmission and understand better the consequences of change in a local context, then we really need to think about understanding the local ecology and the sympatric pairings between those vectors and the parasites." Perspectives on Disease Drivers Global Change and Transmission Risk In the discussion that followed these presentations, and also in comments raised in earlier sessions, several participants expressed concern that disproportionate attention was being paid to the potential influence of climate change on transmission risk for vector-borne diseases, and particularly for West Nile viral disease, where evidence for climate and temperature effects appears particularly thin. "Are we really focusing on the right type of global change by doing so much work on issues around climate change, when really the impact of WNV in the United States may vary with temperature, or it may not?
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Solid empirical data are needed to characterize these relationships. From Models to Mitigation Impressed with the variety and depth of models of vector-borne disease transmission risk, and with Linthicum's Rift Valley fever model in particular, f orum member Julie Pavlin of the Armed Forces Health Surveillance Center asked to what extent these models were being translated into actions that benefited public health.
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"Short of that I think we're just waving our hands, and we can get it completely wrong." On the other hand, Linthicum noted, such high-resolution information may not be necessary to have a significant impact on public health. In Africa, for example, where Rift Valley fever occurs over very large geographic areas affecting many hundreds of thousands of animals, "There's no point in becoming very specific; what you need to do is to warn people when those risks are going to be elevated," he argued, "and then there are a number of things that could be done on a large scale to really mitigate that [threat]
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) Vector control has an important role in addressing vector-borne diseases, observed speaker Paul Reiter of the Institut Pasteur.
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With the banning of DDT, beginning in the 1960s, a new era of insecticidebased vector control began. While DDT had been applied directly to infested containers and their immediate (50 cm)
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"I don't believe that vector control on its own is going to be the answer, even though I'm a medical entomologist. But I do believe that augmentation of the herd immunity by vaccination, in combination with vector control, may prove more effective than either approach on its own." Reiter was emphatic that new and novel approaches to vector control are urgently needed.
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aegypti as the Norway rat of mosquitoes. Because of its intimate association with humans in homes, schools, and work places and its extreme preference for feeding on humans, it is an excellent vector of yellow fever, dengue, and chikungunya viruses, and this mosquito has caused and continues to cause inestimable morbidity and mortality in humans (García-Rejón et al., 2008, 2011)
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Similarly kdr has exploded in Anopheles gambiae threatening the efficacy of long-lasting insecticide-treated nets for malaria control. Pyrethroids are also the insecticide of choice for control of vectors of other globally important diseases such as Chagas, lymphatic filariasis, and leishmaniasis, and they are widely used by public health agencies for control of other insect vectors, such as for those that transmit West Nile virus, and other insect vectors of globally important pathogens.
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New insecticides as well as new innovative strategies for vector control are needed, including insecticide resistance blocking strategies (Devine et al., 2009) , Wolbachia interruption of DENV transmission by Ae.
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To achieve the latter outcome, the Gates Foundation has defined a strategy called Accelerate to Zero, intended to focus current and future tools in an intensive effort to interrupt malaria transmission. The cornerstones of this strategy are the detection of the human parasite reservoir, the elimination of that reservoir, and the effective prevention of transmission, he explained.
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For example, despite the deployment of insecticide-treated bed nets and indoor residual spraying of insecticides, significant residual malaria transmission occurs as mosquito populations adapt both
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Transgenic Insects for Vector Control Effective control strategies for arboviral diseases can target their insect v ectors, observed speaker Luke Alphey of the United Kingdom's Pirbright Insti tute. He described work under way to create and deploy genetically modified Ae.
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. There are two possible goals of genetic control strategies, Alphey explained: to reduce the size of a vector population or to change it in a way that reduces disease transmission -- that is, by somehow reducing vector competence throughout the population.
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While there has been some objection to this trial by environmental activists, an independent pollster found that 61 percent of residents questioned supported the use of genetically engineered mosquito technology, as compared with 18 percent who did not (Florida Keys Mosquito Control District, 2013)
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Managing plant diseases generally requires an integrated approach; therefore, she characterized the methods she described as "just another tool in the toolbox for plant production." Viral Acquisition TSWV, a Bunyavirus, is related to RVFV and other members of the genus Hantavirus, Whitfield noted. TSWV is globally distributed, has an exceptionally wide host range of more than 1,000 plant species, and annually contributes to more than $1 billion in losses of crops that include tomatoes, peanuts, and peppers.
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RNAi for Vector Control Viral-vector interactions could be further exploited as a means of vector control through the use of RNA interference (RNAi) ,22 Whitfield observed (Kupferschmidt, 2013)
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The successful results with RNAi to silence the v-ATPase genes of plant and animal disease insect vectors highlight not only the similarities in basic vector biology but also that of emerging vector control strategies. These commonalities suggest that increased communication and collaboration between investigators working with plant and animal vectors could be beneficial for the control of vector-borne diseases.
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"The first vaccine for horses was approved in 2001," he said. "By that time there were at least six companies engaged in vaccine development for humans," he added -- all of which have since halted their efforts.
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Monath was part of the effort to develop a WNV vaccine at his former employer, Acambis, now owned by Sanofi Pasteur. Their product, ChimeriVaxWN, is a live, attenuated, virus vaccine based on the yellow fever vaccine, which they produced within months of the 1999 outbreak (Dayan et al., 2013)
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[and] in the United States we really don't have any experience with mass immunization campaigns, especially those involving adults." On the other hand, a growing burden of long-term symptoms associated with WNV could tip the scales to justify further vaccine development, Monath observed (Garcia et al., 2014; Maxmen, 2012; Murray et al., 2014)
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Chikungunya's dramatic emergence has raised the profile of a potential vaccine, as does the likelihood that CHIKV will persist for decades in a large human population with abundant mosquito vectors, through which many travelers pass, he noted. There is also the potentially significant burden of chronic, long-term disease.
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and others demonstrates that if you can predict Rift Valley fever activity and immunize the hosts that contribute to amplification of the virus, you can prevent human disease and prevent direct animal-to-human transmission, which may provide a model for other vaccine-preventable diseases. He noted that the approval process for animal vaccines is less onerous than for human vaccines, and therefore potentially a more attractive investment for pharmaceutical companies.
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2004. Emerging infectious diseases of plants: Pathogen pollution, climate change and agrotechnol ogy drivers.
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2006. Assessing capacity for surveillance, preven tion, and control of West Nile virus infection -- United States, 1999 and 2004.
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E Staples, National Center for Emerging Arboviral Diseases Branch, and CDC Zoonotic Infectious Diseases.
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Emerging Infectious Diseases 15(9)
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Emerging Infectious Diseases 11(3)
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Fischer, National Center for Emerging Division of Vector-Borne Diseases, and CDC Zoonotic Infectious Diseases.
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Emerging Infectious Diseases 8:1394-1395.
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2013. Linking environmental drivers to infectious diseases: The European environment and epidemiology network.
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Emerging Infectious Diseases 19(5)
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2015. Disruption of insect transmission of plant viruses.
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