- Countries in the Americas have also historically been leaders in preventing, controlling, and eliminating vector-borne diseases as public health problems. Great examples of this are malaria in the Caribbean, yellow fever in the region, and most recently onchocerciasis from Colombia and Ecuador.
- PAHO has been instrumental, supporting countries in preparedness, prevention, control and elimination of vector-borne diseases, always in collaboration with governments and partners.
- Vector-borne diseases will continue to be a dynamic public health threat to countries in the Americas; therefore, the commitment and financial support from governments and international stakeholders to prevent further spread and strive for elimination is essential.
We are in the early stages of understanding patterns of vector-borne disease (VBD) in animals in the United States and globally. While the enormous impacts of VBD to human and economic health have been well studied, there are unique challenges associated with assessing and controlling VBDs for which an animal host is a major component and even more so when multiple host species can play epidemiologically significant roles.
The scope, relevance, and evaluation of vector-borne pathogens are highly dependent on organizational priorities. No individual list or organization focuses on all VBDs that pose a risk to animals; however, many do cover a portion of viral, bacterial, or parasitic illnesses of relevance. For example, the National Institute of Allergy and Infectious Diseases (NIAID) categorizes infectious agents by their threat to public health and national security. These agents are prioritized and divided into three categories (A, B, and C) based on their transmissibility, potential to cause social disruption, and impact to human health, although many of these pathogens affect animal health as well. Forty percent of the NIAID priority pathogens are vector borne and also widely regarded to infect or cause disease in animals (4 of 18 in Category A, 9 of 24 in Category B, and 13 of 23 in Category C) (NIAID, 2014) (see Table A5-1).
1 Colorado University.
2 EcoHealth Alliance, 460 West 34th Street, New York, USA.
TABLE A5-1 Vector-Borne NIAID Priority Pathogens (Categories A, B, C) That Affect Animals and Humans, OIE-Reportable Terrestrial Mammalian Pathogens, and Viral Families with Novel Primate, Bat, Rodent, and Shrew Viruses Discovered Through the PREDICT Project
Crimean Congo hemorrhagic fever
Eastern equine enchephalomyelitis
Rift Valley fever
Surra (Trypanosoma evansi)
West Nile virus
Nairobi sheep disease
African swine fever
Western equine encephalomyelitis
Equine infectious anemia
Infection with African horse sickness virus
Venezuelan equine encephalomyelitis
Rift Valley fever
Crimean Congo hemorrhagic fever
Typhus fever (Rickettsia prowazekii)
West Nile virus (WNV)
LaCrosse encephalitis (LACV)
Venezuelan equine encephalitis (VEE)
Eastern equine encephalitis (EEE)
Western equine encephalitis (WEE)
Japanese encephalitis virus
St. Louis encephalitis virus (SLEV)
Severe fever with thrombocytopenia Syndrome virus (SFTSV)
Omsk hemorrhagic fever virus
Kyasanur Forest virus
Tick-borne encephalitis complex flaviviruses
Yellow fever virus
Several VBDs are of importance to international trade and are listed as notifiable diseases. One-quarter of the terrestrial vertebrate pathogens of concern to the World Organisation for Animal Health (OIE) are vector borne (OIE, 2014). The goal of the OIE’s list is to promote global transparency and awareness of the condition of animal health to prevent disease introduction or spread.
As these different listings highlight, known VBDs are of great importance and concern to both federal and international organizations for their existing
or potential burden to human and animal health. However, there is no single resource for assessing or prioritizing these VBDs. With the threat of potentially unidentified vector-borne pathogens or pathogens yet to emerge, it is important to recognize this as a shortcoming in our current classifications systems. Over a 5-year period, the PREDICT project, supported by USAID’s Emerging Pandemic Threats program, has identified an additional 36 viruses from taxa that are known to encompass VBDs, suggesting that unknown vector-borne diseases may represent a burgeoning threat to both human and animal health. PREDICT seeks to identify novel zoonotic pathogens before their spread to humans (PREDICT Consortium, 2014), and tests samples from wildlife based on their risk for zoonotic transmission given the ecological setting. Literature review suggests that approximately 40 percent of emerging zoonotic viruses are vector borne (Johnson et al., 2015). Combined, these results point to the importance of VBDs in both animals and humans.
Vector-borne viruses account for 29 percent of the 593 known mammalian viruses (Olival et al., in review). These pathogens have three times the host range compared to nonvector-borne viruses (Johnson et al., 2015) meaning that multiple animal species may act as hosts or reservoirs for any particular VBD. Additionally, individual vector-borne viruses can be transmitted by multiple, related vector species. Not only does this mean that VBDs may broadly affect animal health over a range of species, but it also poses challenges for disease control that targets hosts rather than vectors.
When a VBD affects both people and animals, humans are typically an incidental host and do not serve an important role in transmitting the disease to additional vectors. However, this does not exclude humans from being affected both directly and indirectly by VBDs for which they are not the primary host. VBDs can have serious effects on human and animal health as well as significant economic implications.
While climate change is commonly cited as a major contributor to increasing VBD prevalence and distribution, it is important to recognize that numerous human and ecological factors play a major role in disease emergence and spread. Patterns of VBDs can be attributed to a wide range of variables that vary by disease, location, and circumstance (see Figure A5-1). Additionally, identifying the drivers that are associated with VBD emergence and spread presents an opportunity for prevention, education, and control. Changes in land use, war and famine, breakdown of public health measures, global trade and travel, and human behavior are all associated with VBD emergence (Loh et al., 2015) (see Figure A5-2). By identifying situations where we anticipate VBD emergence, we can more effectively target prevention and intervention strategies.
Recent VBD emergence events have highlighted the important role of animal hosts or reservoirs. We examine four examples, Schmallenberg virus, West Nile virus, tick-borne illness, and Rift Valley fever virus, for their trends and implications in terms of animal health.
Schmallenberg virus (SBV) is a novel nonzoonotic virus in the Bunyaviridae family that emerged in Germany and the Netherlands in 2011 and is now reported in most European nations. It primarily affects domestic ruminants and has been detected serologically in dogs and a number of wildlife and zoo species including alpaca, water buffalo, elk, bison, red deer, fallow deer, roe deer, muntjac, and chamois (Sailleau et al., 2013; EFSA, 2014). Biting midges, Culucoides spp., are the primary vectors (EFSA, 2014), which likely dispersed throughout Europe via wind-mediated spread (Sedda and Rogers, 2013). Although midges do not easily acquire SBV from infected sheep, and the prevalence of the virus in midges is low at 0.25 percent (Elbers et al., 2013), biting midges are efficient at transmitting the virus to animals, with a 0.76 probability of transmission from an infected vector to host (EFSA, 2014).
The basic reproduction number (R0) of Schmallenberg is 5–7 per infected animal, which peaks at 21°C (see Figure A5-3). This high value for R0 follows
suit with similar VBDs; however, the temperature for optimal transmission is relatively mild. Indeed, warmer conditions are not universally optimal for all vector-borne diseases, and additional factors must be considered when addressing VBD spread on a whole.
SBV does not generally kill sheep, and currently it is not a notifiable disease to the OIE. However, non-OIE related international trade restrictions due to SBV have had major implications for the EU’s live animal and bovine semen trade, resulting in serious economic consequences. For example, in 2012, SBV was responsible for an 11–26 percent decline in bovine semen exports to non-EU countries and a 20 percent decline in breeding animal exports from €590 million to €475 million (EFSA, 2014).
While symptoms in affected cattle and sheep are generally rare, clinical signs of acute SVB infection can cause fever, reduced milk yield, diarrhea, and abortion. The animal typically recovers in 4–6 days, after which it is immune (Meroc et al., 2014). The rate of abortions in SBV infected flocks is double compared to uninfected flocks, with a five-fold increase in malformations (Saegerman et al., 2014). Obstructed labor in domestic ruminants imposes additional draining of resources from farmers and veterinary professionals as a result of the work in assisting with birth. Fifteen percent of SBV infected pregnant ewes have obstructed labor, and 2 percent die as a result (Dominguez et al., 2012). This loss can impose a major burden on affected farmers who operate on small profit margins.
Current strategies for mitigation of midge-borne viruses include vector control, timed breeding, and vaccination. Midge control through the use of pesticides is largely impractical both for the individual farmer and for large-scale
prevention of disease. Breeding before or after the midge season is also uncertain, as expansions in vector range or longer peak midge season may have implications for the usefulness of this method (Wittmann et al., 2002; Wernike et al., 2013a,b). Available vaccines suggest promise for SBV control. However, the marketability of these immunizations is questionable. There is marginal incentive for livestock owners to purchase the vaccines and hence for pharmaceutical companies to promote them. Given the overall mild symptoms, short duration of illness in domestic ruminants, and the gain of immunity postrecovery it may not be economically viable to vaccinate. Individual livestock owners will most likely have to live with the burden of disease unless improved control strategies become available.
West Nile Virus: Shifts in Surveillance
Patterns of West Nile virus (WNV) emergence and transmission are highly dependent on a wide range of variables, many of which are stochastic or unpredictable. While landscape and weather factors do play a role in transmission dynamics, it is impossible to discuss patterns of WNV emergence without addressing the dramatic changes in surveillance throughout the history of the virus in the United States. From 2004 to 2012 there was a 61 percent reduction of CDC epidemiology and laboratory capacity (ELC) funding which affected state- and county-level WNV surveillance in their early detection capacity and ability to determine and monitor patterns of the virus in animals and humans (Hadler et al. 2014) (see Figure A5-4).
To function effectively, consistent support is needed in surveillance activities, as geographically patchy surveillance limits our ability to draw conclusions on trends or correlations with factors that may affect disease prevalence (see Figure A5-5). WNV is far from the only vector-borne disease for which lapses in testing and reporting leaves gaps in our understanding of pathogen dynamics. Lyme disease in dogs, discussed later in this report, is also a valuable example of how gaps in surveillance affect our ability to monitor disease trends.
When addressing WNV control in domestic animals, our competitive marketing strategies may interfere with optimal surveillance. There are currently two WNV vaccines available for veterinary use in the United States; however, vaccine use in the United States is confidential information, and sales data are regarded as proprietary. We are therefore lacking critical knowledge regarding disease control in domestic animals. It would be of benefit to the public health community to have information regarding the geographic distribution and volume of vaccines used to detect potential trends or changes over time. A network for immunization use across the United States would aid the public and animal health community in our understanding of where disease control is being implemented and our ability to take action in emerging areas for control.
Tick-Borne Diseases in Companion Animals and Livestock
Pathogens transmitted via tick bite, or tick-borne diseases (TBDs), broadly affect domestic animals, livestock, and wildlife worldwide. Ticks feed on a wide range of animal taxa including mammals, reptiles, amphibians and birds, often using different hosts throughout their life cycle, creating multiple opportunities for disease spread between species.
Geographic patterns of Lyme disease (Borrelia burgdorferi) prevalence in dogs have closely followed those in humans, with the highest regions of seroprevalence occurring in the United States northeast and Midwest, where some clusters have seroprevalence as high as 44.1 percent. A comparison of studies of Lyme disease seroprevalence in domestic dogs in the United States showed an increase from 11.2 percent in the 2001–2007 study period to 13.3 percent in the 2010–2012 study period (Bowman et al., 2009; Little et al., 2014) (see
Figure A5-6). Because of the interconnectedness of humans and domestic dogs, it can be expected that patterns for Lyme disease would be similar among both. Human activity and other ecological drivers are likely responsible for these increases of disease prevalence; however, the role of inadequate surveillance in our ability to perceive these patterns must be addressed. A lack of centralized reporting for canine Lyme disease makes it difficult to discern whether these parallel increases
are a function of a change in the amount of diagnostic testing or actual shift in disease range. Gaps in uniform surveillance of TBD in companion animals impede accurate and integral epidemiologic monitoring, particularly in nonendemic regions (see Figure A5-6).
Whereas ectoparasiticides are relatively easy to administer to companion animals for tick control, managing ticks and TBD in the livestock industry is a major challenge both to individual farmers and on the global scale. TBD affects 80 percent of the world’s livestock holdings, and the economic cost of TBD is $13.9 billion to $18.7 billion annually (Minjauw and McLeod, 2003). This economic burden can be substantial in resource-poor tropical and subtropical regions, particularly to small-scale livestock owners (Minjauw and McLeod, 2003). The cost of controlling TBD in some areas exceeds animal production costs, as is seen with theileriosis in Tanzania (see Figure A5-7). The significant burden is especially pertinent when adherence to international standards for vector control at national levels is a trade requirement.
A One Health Approach to Vector-Borne Diseases—RVF as an Example
Rift Valley fever (RVF) is an emerging mosquito-borne zoonotic disease and has been recognized as a pathogen of significant concern by the WHO, OIE, FAO, U.S. CDC, U.S. DoD, and USDA, with broad relevance for both human health and livestock production. The virus has caused large epizootics in Africa, and has recently led to outbreaks in the Middle East. RVF outbreaks are devastating to domestic ruminants, in which it causes widespread abortions and high mortality (> 90 percent in some cases) in juveniles (Murphy et al., 1999). Infection in humans can occur through the bite of an infected mosquito or via contact with tissues or bodily fluids from an infected animal.
RVF outbreaks have been extensively studied in Kenya, where it was first discovered in 1931. East African RVF outbreaks appear to occur periodically (in cycles every 7–15 years), with little to no activity during interepidemic periods, and are associated with heavy floods. This RVF virus cycle involves a sylvatic cycle with transmission between Aedes mosquitos and wild and domestic ruminants; the mosquitoes can transmit it transovarially. Wild and domestic ruminants typically experience subclinical infections in interepidemic periods, but heavy rains increase Aedes populations, leading to amplification in domestic ruminants, and increasing potential for outbreaks in domestic ruminants and transmission to humans.
While this weather-dependent cycle is well established in Kenya, outbreaks appear to be less cyclical, or have different determinants, in South Africa. A recent analysis of outbreaks showed RVF outbreaks of varying scales and in different regions reported in South Africa each year from 2008–2011 (Metras et al., 2012). The scale of infection and spread may be a major consideration for immunity, with apparent low immunity in interepidemic periods, and potential herd immunity established during outbreaks. However, despite potential mixing of wildlife and domestic animals at some ranch sites (whether through presence of farmed wildlife or via free-ranging wildlife at the periphery of farms), the role of wildlife—if any—in the infection cycle and resulting immunity for wildlife and domestic animals has not been widely studied. The potential role of
burden on mosquitos, domestic animals, wildlife, humans, and ecological factors (e.g., climate) in RVF show the complexity of some VBDs. Thus, an integrated approach is needed to better understand interspecies and other transmission dynamics.
A One Health approach that considers the links between humans, animals, and the environment can thus provide a more robust view around causes and possible solutions to VBDs such as RVF. A unique U.S. Department of Defense (DoD) DTRA-supported partnership between EcoHealth Alliance, the South African National Institute for Communicable Diseases, South African National Parks, the Free State Province Department of Economic Development, Tourism and Environmental Affairs, Republic of South African Department of Defence, University of Pretoria, and NASA/Universities Space Research Association has been established under a 5-year comprehensive study of RVF in South Africa. The project, which has a strong capacity-building component, will allow for a greater epidemiological understanding of RVF dynamics through four central aims: (1) Determine how immunity to RVFV changes over time in sheep; (2) determine the herd immunity in wildlife and domestic animals; (3) understand the ecology of the virus in the mosquito vector; and (4) determine the immunity level in people working on the study farms and detect new infections. By employing different vaccination scenarios in flocks to study herd immunity, studying prevalence of natural infection and epidemiological risk factors, investigating mosquito abundance and succession, and using climate, vegetation and soil data, we will gain a greater ability to better predict potential outbreaks in the future. Additionally, by enhancing knowledge on herd immunity at individual, population, and metapopulation levels, information obtained from this project will enable more targeted vaccination and mitigation methods for RVFV. This project will involve a 40,000 square km study site in the Free State and the Northern Cape province. The study will monitor humans, cattle, sheep, goats, and selected species of wildlife; assess the presence of RVFV throughout the life cycle of multiple mosquito species; and analyze mosquito blood meals to determine which species the vectors prefer. Additionally, the project will link patterns of human, animal, and mosquito occurrence with weather and vegetation cycles. This broad-based approach will hopefully provide a more comprehensive epidemiological understanding of RVFV as it pertains to wild and domestic animals, vectors, people, and the environment.
For the future, we can say with confidence that known VBDs will continue to be a significant disease burden for animals and people, and new VBDs will continue to be identified. We are even witnessing VBD affecting endangered species recovery programs; for example, Yersinia pestis, has been a major barrier to the recovery of black-footed ferret populations (Godbey et al., 2006). There is no indication that vector-borne disease is going to be eliminated in the near future. Current methods of VBD classification are highly dependent on organizational priorities with a strong focus on direct and indirect impacts to human health and a segregation of VBDs of animal importance.
The ability to discern patterns of VBD in animals hinges on consistent surveillance, prioritization, and integrative strategies. It would be an immense and inappropriate undertaking to attempt to eliminate ticks, mosquitoes, fleas, and midges in order to prevent VBDs. While vaccines present an opportunity at the individual animal or herd level, the associated cost-benefit relationships poses additional challenges. To better understand and control VBDs, we need more than molecular diagnostics and new or better vaccines. A fundamental quality of VBDs, their dependence on the ecology of vectors and hosts, points to the need for the earnest engagement of the ecological sciences. Skilled medical entomologists are critical for future work, and the number in this field are dwindling. There is an urgent need for ongoing support and training in medical entomology to meet emerging demands.
The possibility and opportunity for introduction of VBDs on a global scale cannot be ignored. As was seen with the emergence of WNV in South Dakota, the favorable ecological conditions for disease emergence cannot always be predicted. Controlling VBDs can be expensive and labor intensive. With the 10-year anniversary of One Health behind us, it is important to pull together thinking on human, animal, and plant vector-borne illness to find synergistic collaborative interventions to benefit health as a whole.
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