Abstract
Newly emerging or re-emerging infections continue to pose significant global public health threats. This chapter provides an overview of the combinations of factors that led to the emergence of arthropod-borne viruses as human and veterinary health threats, in order to understand the risk associated and how this can be mitigated. Considering the history of emergence of some arboviruses, these epidemics have occurred globally as a result of climate and socioeconomic changes that have allowed the spread to new geographical areas of viruses previously confined to specific ecological niches such as West Nile and Chikungunya, or viruses considered under control such as Dengue, Japanese encephalitis, and Yellow fever. Moreover, the greatest risk for humans derives from the ability of these viruses to adopt transmission cycles involving highly anthropophilic mosquito species. Finally, many other arboviruses are largely ignored despite their potential to emerge globally. The recent epidemic spread of Zika virus throughout the Americas is the evidence that arboviruses are likely to continually emerge and re-emerge and that improved scientific technologies and knowledge is essential to deal with future vector-borne epidemics. Research priorities should therefore focus on surveillance systems and vector control tools, as well as on the development of antiviral molecules or candidate vaccine.
Keywords
- arbovirus
- emerging infectious diseases
- dengue
- Chikungunya
- yellow fever
- West Nile
- Zika virus
1. Introduction to arboviruses
Arthropod-borne viruses (arboviruses) are important cause of animal and human disease worldwide, infecting millions of individuals and causing a large social and economic burden. These viruses are generally transmitted by arthropod vectors to their vertebrate host and circulate among wild animals serving as reservoir in sylvatic life cycle. Through spillover transmission from enzootic amplification cycles, humans can be infected as incidental and dead-end hosts. By contrast, some arboviruses undergo urban cycle involving humans as amplifying hosts and causing several epidemics in urban areas [1, 2, 3].
By definition, arboviruses require an arthropod vector in the transmission cycle, in which they must replicate prior to transmission [1]. Most common arthropods include mosquitoes, flies, and ticks along with others hematophagous arthropods [2, 3].
Most of the arboviruses that cause human/animal diseases belong to four virus families,
A high proportion of arboviruses associated with human and animal disease circulate in tropical and subtropical regions, where arthropods tend to be abundant. However, many arboviruses also circulate among wildlife species in temperate regions of the world. Despite the global distribution of viruses such as West Nile virus (WNV), DENV and now CHIKV, most other arboviruses are generally endemic but limited to specific regions of the world. Nevertheless, even within this relatively localized distribution, dispersion to distant locations can occur via animal or vector migration [4]. Global warming, deforestation, and urbanization have led to rapid expansion of the habitats of the vectors and caused enormous increase in vector-borne diseases throughout the world. Increase in international travel, shipping, and industrialization can lead to transport of infected mosquito and eggs to different new ecological niches facilitating the contact with naïve individuals causing outbreaks of high magnitude due to lower herd immunity [2]. The greatest health risk of arboviral emergence comes from extensive tropical urbanization and the colonization of this expanding habitat by the highly anthropophilic mosquito,
More than 500 species of viruses are registered in the International Catalog of Arboviruses and this estimate is continuously increasing. While many current arboviruses do not appear to be human or animal pathogens, this large number of widely different and highly adaptable arboviruses provides an immense resource for the emergence of new pathogens in the future [4].
2. Emerging and re-emerging arboviral infections
2.1. Factors associated with arbovirus emergence or invasion
Recent global changes in climate and human behavior are important determinants of arbovirus emergence. The viral transmission can be limited by the ecology of the host or of the virus itself; arboviruses frequently persist at low maintenance levels until changes in single or multiple factors disrupt the transmission cycle, facilitating rapid and widespread amplification [1, 6]. Arboviruses can therefore emerge at epidemic levels due to changes in viral genetics, in the composition or dynamics of the host or vector population and/or in the environmental structure that often are of anthropogenic origin [1].
As arboviruses are virtually all RNA viruses lacking proofreading functions, a high frequency of mutations associated with fast replication allows them to rapidly adapt to different environments. The high rate of genetic mutations could lead to changes in virulence, epidemiology or competence of vectors, which can occur via simple point mutations [3, 5]. Often, outbreaks of emerging arboviruses may be related to relatively small changes in viral genetics or to the introduction of new strains that have increased virulence and viremia levels in vertebrate, thereby expanding the host range and increasing amplification potential. Alternatively, genetic changes can improve vector competence and therefore transmission rates [1].
Zoonoses exploiting complex rural or suburban ecosystems may have multiple vectors and infect a variety of vertebrate host species. Arboviral amplification can progress rapidly to epidemic levels when competent vector and vertebrate host populations meet repeatedly within a permissive environment for viral transmission and replication. Moreover, humans may be exposed to arboviruses when they invade rural environments or when bridge vectors bring viruses into peridomestic environments [1]. Deforestation associated with urbanization process has contributed to increase the contact between humans and vectors [7]. Furthermore, the expansion of urbanization has led to high concentrations of susceptible human hosts, often living in socioeconomic conditions favorable to the expansion of the vector population, facilitating viral transmission and outbreaks of epidemics [1]. Furthermore, the feeding preferences (anthropophilic and/or ornithophilic) of arthropod vectors are of fundamental importance [8, 9, 10]. Arthropods frequently exposed to the human environment, domestic animals, and livestock can undertake an adaptive process defined as domestication [8, 11]. Moreover, many of the epidemic vectors are peridomestic, naturally existing in close association with humans. The vectors of CHIKV, YFV, and Zika virus (ZIKV) all use human habitat to maintain their populations [12, 13]; thus, general living conditions along with ineffective vector control programs, can contribute to providing one component necessary for arboviral transmission [5, 7].
Changes in the composition of vertebrate or vector host species may be related to environmental changes that expand old or create new ecological niches. Extensions of the vector range into permissive environments are often followed by invasion of the arboviruses they transmit. These invasions are generally facilitated by travel and commerce [1], constantly introducing new species of viruses and their arthropod vectors into new geographic areas. Most of these introductions are not detected until they cause an epidemic, when they are already well established and it is not possible to eliminate them from the new area [7]. An additional factor that plays a role in the generation of arboviral outbreaks is the immunity status of vertebrate hosts in the affected areas. Outbreaks registered for the first time in a new area usually involve immunologically naïve populations, exhibiting extremely high rates of attack. Even in areas where epidemics have previously occurred, rare epidemic events interspersed with significant interepidemic periods may render the younger generation susceptible to infection [5].
Following their recent local and global emergence, some arboviruses have acquired great importance in terms of public and veterinary health. The combinations of factors that led to their emergence are of fundamental importance to understand the risk associated and how this can be mitigated. Moreover, many other arboviruses are largely ignored despite their potential to emerge globally [1].
2.2. Emerging and re-emerging arboviruses
2.2.1. Dengue virus
DENV (
2.2.2. Chikungunya virus
CHIKV is an
2.2.3. Zika virus
ZIKV (
2.2.4. Yellow fever virus
YFV is the type of species in the
2.2.5. West Nile virus
WNV belongs to the Japanese encephalitis virus (JEV) serocomplex in the genus
2.2.6. Japanese encephalitis virus
JEV is the most frequent cause of mosquito-borne encephalitis globally. The public health significance and the global distribution of JEV have been progressively expanding; currently, more than 3 billion people in Asia reside in areas at risk of JE, with an estimated 50,000 symptomatic cases and 10,000 deaths occurring annually [46]. Taxonomically, JEV is placed within the genus
2.3. Arboviruses with potential of emergence
2.3.1. Rift Valley fever virus
Rift Valley fever virus (RVFV) is classified within the genus
2.3.2. Mayaro virus
Mayaro virus (MAYV) is an emerging
2.3.3. Venezuelan equine encephalitis virus
Venezuelan equine encephalitis virus (VEEV) is an alphavirus (
3. Strategies for arbovirus control
Because they are not an essential part in the zoonotic arbovirus life cycle, arbovirus disease control based on humans and domestic animals cannot eradicate the arbovirus. Consequently, the reservoir in wild species places a limitation in the control disease emergence, and only understanding the interactions involved in the biology of the virus, hosts, and ecology will lead to effective control and prevention strategies [4, 5]. With effective vaccination and sustainable vector control programs, it is possible to control or even eliminate human transmission cycles. In fact, vaccination can increase herd immunity, making it easier to sustain reduced virus transmission with vector control. On the other hand, vector control can complement a vaccine by lowering the risk of infection, making vaccine delivery goals easier to achieve [75].
The YF vaccine has been used extensively in West Africa and has been instrumental in eliminating the urban transmission cycle in South America. However, despite its efficacy and low-cost production, epidemics continue to occur due to inadequate vaccination coverage, as demonstrated by the recent YF outbreak in Angola and Democratic Republic of Congo [76]. Adequate and continuous vaccination programs along with high levels of herd immunity are of paramount importance for the control of YF. In Africa, together with childhood immunization, mass preventive vaccination campaigns to protect elderly people need to be implemented [77]. Moreover, in South America, people of coastal areas are largely unvaccinated and therefore exposed to the risk of YFV coming from the near enzootic regions [75]. Finally, YF cases reported from travelers from Angola to China highlight the need to implement the WHO International Health Regulations in order to protect travelers and to avoid the introduction of YFV in naïve areas of Asia where the vector is widely present [76]. Japanese encephalitis was controlled in Japan, Taiwan, and Korea using inactivated vaccines, which also contributed to control infection in China [10, 78]. A live attenuated JEV vaccine was used to reduce the risk of infection in children in China, as well as being part of the large children immunization campaign in India [10]. At the end of 2015, the first dengue vaccine was licensed (CYD-TDV vaccine Dengvaxia). The results of a large phase III study in 10 endemic countries in Asia and South America showed a complex performance of the vaccine with efficacy dependent on serotype, as well as previous immunity and age of the subject [79, 80]. Two other live dengue virus vaccines are in phase III trials and many other dengue vaccines are in phase I and II trials [75]. Research on vaccines against CHIKV has been slow, as CHIKV causes major epidemics only every 10–30 years, limiting the interest of the pharmaceutical industry for a financial return [75]. However, two vaccines against CHIKV have recently completed phase I clinical trials, both are strongly immunogenic after 2–3 doses and are currently in phase II trials [81, 82]. Among more than 40 Zika vaccines developed, DNA, RNA, and inactivated virus [83, 84, 85] versions started clinical trials and the first live-attenuated vaccine has been demonstrated to be safe and efficacious after a single dose in mice [86]. However, there are some concerns about potential interactions with immunity generated by other flavivirus natural infections or vaccines leading to more severe manifestations of the disease, as well as the immune trigger in the development of Guillain-Barre syndrome [87]. Currently, there is no specific licensed anti-arbovirus agent, and patient management is therefore mainly supportive. Passive immunotherapy is a promising approach for the management of newborns exposed to CHIKV. The anti-CHIKV human immunoglobulins purified from convalescent donors exhibit strong anti-CHIKV effects in vitro and animal models [88], and are now evaluated in the prevention of mother-to-child CHIKV transmission in newborns born to viremic mothers [87]. Novel antiviral therapies are also being investigated. Drug repurposing strategies have identified potential inhibitors of
The continued outbreaks of YFV and JEV demonstrate that even with a widely available and effective vaccine, it is difficult to control a vector-borne disease using only vaccination [6]. Overall, the best current perspectives for controlling the majority of vector-borne diseases rely on reducing the contact between the vector and susceptible humans and the most effective approach for this goal remains the elimination or reduction of mosquito populations [87]. Nowadays, many of the insecticides used in the mid-twentieth century eradication campaign are considered environmentally unacceptable, as well as being economically prohibitive and at risk of developing resistance in mosquito populations [87, 91]. Several alternative approaches are focused on reducing the abundance of mosquitoes or preventing the transmission of pathogens by the mosquito. Environmental management includes modification of the natural breeding habitat of mosquitoes and the adoption of human behaviors that reduce the incidence of the bite, such as the elimination of domestic oviposition and larval sites, the indoor residual spraying and fumigation, the use of insecticide-treated bed nets and screening windows together with lethal traps, which have been found to be effective in reducing
The implementation of localized arthropod control measures during epidemics, for example, in high-density urbanized areas, can play an important but transient role in reducing the impact on humans and animals of emerging arboviruses if these are supported from surveillance systems, which differ at regional level and in many areas are completely absent [4]. Furthermore, it is essential to characterize and understand viral genetics, antigenic properties, virulence patterns, vector associations, and maintenance mechanisms to identify and control future arboviral outbreaks. The next public health needs include communication to the population and physicians of vector-borne diseases, the guarantee of vector control programs, and the maintenance of adequate surveillance systems with trained personnel, together with the availability of drugs, vaccines, and rapid diagnostic testing [5].
4. Conclusions
Arboviruses already have a well-known history of emergence and will undoubtedly continue to emerge in the future. There are many unidentified arboviruses that, due to their high mutation rates, may emerge as pathogens even if they are not yet present as epidemic strains in the wild environment. Recent progress in sequencing offers new opportunities to identify them during surveillance activities, especially in the tropics, where viral diversity is higher [3]. The greatest risk for humans derives from the ability of some arboviruses to adopt urban transmission cycles involving highly efficient and anthropophilic vectors, such as
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