Elsevier

Antiviral Research

Volume 85, Issue 2, February 2010, Pages 328-345
Antiviral Research

Review
Present and future arboviral threats

https://doi.org/10.1016/j.antiviral.2009.10.008Get rights and content

Abstract

Arthropod-borne viruses (arboviruses) are important causes of human disease nearly worldwide. All arboviruses circulate among wild animals, and many cause disease after spillover transmission to humans and agriculturally important domestic animals that are incidental or dead-end hosts. Viruses such as dengue (DENV) and chikungunya (CHIKV) that have lost the requirement for enzootic amplification now produce extensive epidemics in tropical urban centers. Many arboviruses recently have increased in importance as human and veterinary pathogens using a variety of mechanisms.

Beginning in 1999, West Nile virus (WNV) underwent a dramatic geographic expansion into the Americas. High amplification associated with avian virulence coupled with adaptation for replication at higher temperatures in mosquito vectors, has caused the largest epidemic of arboviral encephalitis ever reported in the Americas. Japanese encephalitis virus (JEV), the most frequent arboviral cause of encephalitis worldwide, has spread throughout most of Asia and as far south as Australia from its putative origin in Indonesia and Malaysia. JEV has caused major epidemics as it invaded new areas, often enabled by rice culture and amplification in domesticated swine. Rift Valley fever virus (RVFV), another arbovirus that infects humans after amplification in domesticated animals, undergoes epizootic transmission during wet years following droughts. Warming of the Indian Ocean, linked to the El Niño-Southern Oscillation in the Pacific, leads to heavy rainfall in east Africa inundating surface pools and vertically infected mosquito eggs laid during previous seasons. Like WNV, JEV and RVFV could become epizootic and epidemic in the Americas if introduced unintentionally via commerce or intentionally for nefarious purposes. Climate warming also could facilitate the expansion of the distributions of many arboviruses, as documented for bluetongue viruses (BTV), major pathogens of ruminants. BTV, especially BTV-8, invaded Europe after climate warming and enabled the major midge vector to expand is distribution northward into southern Europe, extending the transmission season and vectorial capacity of local midge species.

Perhaps the greatest health risk of arboviral emergence comes from extensive tropical urbanization and the colonization of this expanding habitat by the highly anthropophilic (attracted to humans) mosquito, Aedes aegypti. These factors led to the emergence of permanent endemic cycles of urban DENV and CHIKV, as well as seasonal interhuman transmission of yellow fever virus. The recent invasion into the Americas, Europe and Africa by Aedes albopictus, an important CHIKV and secondary DENV vector, could enhance urban transmission of these viruses in tropical as well as temperate regions. The minimal requirements for sustained endemic arbovirus transmission, adequate human viremia and vector competence of Ae. aegypti and/or Ae. albopictus, may be met by two other viruses with the potential to become major human pathogens: Venezuelan equine encephalitis virus, already an important cause of neurological disease in humans and equids throughout the Americas, and Mayaro virus, a close relative of CHIKV that produces a comparably debilitating arthralgic disease in South America. Further research is needed to understand the potential of these and other arboviruses to emerge in the future, invade new geographic areas, and become important public and veterinary health problems.

Section snippets

Introduction to the arboviruses

Arthropod-borne viruses (arboviruses) are transmitted biologically among vertebrate hosts by hematophagous (blood feeding) arthropod vectors such as mosquitoes and other biting flies, and ticks. Being, by definition, biologically transmitted, arboviruses must replicate in the arthropod vector prior to transmission, as opposed to being mechanically transmitted, without replication in the vector, through contaminated mouthparts (Weaver, 1997). Biological transmission can be vertical, involving

Factors associated with arbovirus emergence or invasion

For arboviral amplification to progress rapidly to epidemic levels, competent vector and vertebrate host populations must intersect repeatedly within a permissive environment. This focus or nidus of transmission may be temporally and/or spatially constrained by host or virus ecology, and may vary in complexity depending upon virus epidemiology. Zoonoses exploiting complex rural or suburban ecosystems may have multiple vectors and infect a variety of vertebrate host species, whereas

Distribution and health significance

West Nile virus (WNV) is positioned taxonomically within the Japanese encephalitis virus (JEV) serocomplex in the genus Flavivirus. It is maintained and amplified in nature within an enzootic transmission cycle among passeriform birds and Culex mosquitoes, with outbreaks caused by tangential or spillover transmission to equids and humans, ‘dead-end’ hosts that produce viremias inadequate for mosquito infection. WNV is distributed circumglobally, with two main genetic lineages: Lineage 1 is

Distribution and health significance

Dengue viruses comprise four related serotypes that share common transmission cycles (Fig. 5). They are flaviviruses (Flaviviridae: Flavivirus) closely related to JEV and WNV described above; however, unlike all other flaviviruses, DENVs that cause most human disease are not zoonoses, but exclusively utilize humans as reservoir and amplification hosts. Also unlike most arboviruses, they rely on transmission by mosquito vectors that live in close association with people; Ae. (Stegomyia) aegypti

Examples of other arboviruses with the potential for urban emergence

There are many known and probably even more unknown arboviruses with the potential for epidemic emergence, especially as climate change and urbanization enhance opportunities for spread and interhuman transmission. We include here a few of many examples of each emergence.

Conclusions

Arboviruses have a well-documented history of emergence through several mechanisms, including geographic expansion, often mediated through human transportation, and enhanced amplification in peridomestic commensal and domesticated animals leading to spillover to humans. Both of these mechanisms threaten to increase in the future due to increased human travel and global commerce as well as deforestation and tropical human population growth. Global warming also has the potential to increase the

Acknowledgments

The authors’ research is supported by NIH grants AI069145, AI25489 and AI071192 (SCW) and AI055607 (WKR), NASA grant 05-DEC05-S2-0016 (WKR) and CDC grant U01 EH000418-01 (WKR).

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